Dynamic exchanges between DOM and POM pools in coastal and inland aquatic ecosystems: A review

Science of the Total Environment 551–552 (2016) 415–428

Contents lists available at ScienceDirect

Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

Review

Dynamic exchanges between DOM and POM pools in coastal and inland aquatic ecosystems: A review Wei He a, Meilian Chen a, Mark A. Schlautman b, Jin Hur a,⁎ a b

Department of Environment and Energy, Sejong University, Seoul 143-747, South Korea Department of Environmental Engineering and Earth Sciences, Clemson University, Anderson, SC 29625-6510, United States

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• DOM-POM exchanges are dynamic with various ecosystem processes involved. • A micro-spatial mechanistic schema is clearly presented for the complex phenomena. • Influencing factors are critically evaluated from ecological and molecular perspectives. • A unified conceptual model based on exergy theory is proposed to integrate all processes.

a r t i c l e

i n f o

Article history: Received 25 November 2015 Received in revised form 3 February 2016 Accepted 4 February 2016 Available online 13 February 2016 Editor: D. Barcelo Keywords: Dissolved organic matter (DOM) Particulate organic matter (POM) Exchange mechanism Aggregation Adsorption Exergy

⁎ Corresponding author. E-mail address: [email protected] (J. Hur).

http://dx.doi.org/10.1016/j.scitotenv.2016.02.031 0048-9697/© 2016 Elsevier B.V. All rights reserved.

a b s t r a c t Dynamic exchanges between dissolved organic matter (DOM) and particulate organic matter (POM) plays a critical role in organic carbon cycling in coastal and inland aquatic ecosystems, interactions with aquatic organisms, mobility and bioavailability of pollutants, among many other ecological and geochemical phenomena. Although DOM-POM exchange processes have been widely studied from different aspects, little to no effort has been made to date to provide a comprehensive, mechanistic, and micro-spatial schema for understanding various exchange processes occurring in different aquatic ecosystems in a unified way. The phenomena occurring between DOM and POM were explained here with the homogeneous and heterogeneous mechanisms. In the homogeneous mechanism, the participating components are only organic matter (OM) constituents themselves with aggregation and dissolution involved, whereas OM is associated with other components such as minerals and particulate colloids in the heterogeneous counterpart. Besides the generally concerned processes of aggregation/dissolution and adsorption/desorption, other ecological factors such as sunlight and organisms can also participate in DOMPOM exchanges through altering the chemical nature of OM. Despite the limitation of current analytical technologies, many unknown and/or unquantified processes need to be identified to unravel the complicated exchanges of OM between its dissolved and particulate states. Based on the review of several previous mathematical models, we proposed a unified conceptual model to describe all major dynamic exchange mechanisms on the basis of exergy theory. More knowledge of dynamic DOM-POM exchanges is warranted to overcome the potential

416

W. He et al. / Science of the Total Environment 551–552 (2016) 415–428

problems arising from a simple division of OM into dissolved versus particulate states and to further develop more sophisticated mathematic models. © 2016 Elsevier B.V. All rights reserved.

Contents 1. 2. 3.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ecosystem-level perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conceptual models of exchange mechanisms . . . . . . . . . . . . . . . . . . . . . . . 3.1. Aggregation/dissolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Adsorption/desorption . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Photo-induced exchange . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4. Organism-involved exchange . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Main influencing factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Physico-chemical factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1.1. Properties of organic matters . . . . . . . . . . . . . . . . . . . . . . . 4.1.2. Light, temperature, and redox environment . . . . . . . . . . . . . . . . . 4.1.3. Ions (multivalent cations, pH, total alkalinity, inorganic nutrients, and salinity) . 4.1.4. Hydrodynamic factors . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Biotic factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. DOM-POM exchanges in mathematical models . . . . . . . . . . . . . . . . . . . . . . . 6. Summary and future prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Appendix A. Supplementary data. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction Natural organic matter (NOM) is ubiquitous on Earth, including approximately 662 Gt of dissolved organic carbon stored in the ocean (Hansell et al., 2009). This total amount of aquatic NOM rivals the carbon storage in terrestrial soil environments (1200–1600 Gt) (Post et al., 1990). Due to climate change caused by anthropogenic activities, stocks of aquatic NOM are showing increasing trends with the primary sources of NOM originating from land although it is leveling off in the Northern hemisphere (i.e., allochthonous NOM) (Evans et al., 2005; Roulet and Moore, 2006; Monteith et al., 2007; Oulehle and Hruška, 2009). Global stock changes of NOM in aquatic ecosystems (marine, estuarine, riverine, and limnic ecosystems, etc.) are expected to lead to variations of carbon transport and aquatic productivity (Bacastow and Maier-Reimer, 1991; Kepkay, 1994). As part of the sources from living organisms' exudation and detritus (Wetzel, 1995; Passow, 2002), NOM plays a “bridging” role between living and nonliving systems (Verdugo et al., 2004; Azam and Malfatti, 2007), contributing to the maintenance of the aquatic food web by providing foods and energy to heterotrophic microorganisms (Grossart and Simon, 1998; Zimmermann-Timm, 2002; De La Rocha et al., 2008). NOM also influences environmental behaviors of pollutants by affecting their solubility, toxicity, bioavailability, mobility, and ultimate fate (Eadie et al., 1992; Eriksson et al., 2004; Hassett, 2006), and attenuates harmful light by scattering and absorbing (Schindler and Curtis, 1997). In practice, NOM is often categorized and quantified as dissolved organic matter (DOM) or particulate organic matter (POM) based on filtering. A filter pore size of 0.45 μm is typically utilized to set the operational boundary between DOM and POM, although various researchers may use filter pore sizes ranging from ~ 0.1 to ~ 0.7 μm (Verdugo et al., 2004; Roulet and Moore, 2006; Azam and Malfatti, 2007). In the oceans, estimated stocks of carbon from DOM and POM are 662 Gt and 30 Gt, respectively (the conversion factor is variable between 1.5 and 6 to convert POC or DOC into POM or DOM) (Hansell et al., 2009; Post et al., 1990). The dynamic exchanges between DOM and POM plays critical roles in organic carbon cycling (Chin et al., 1998; del Giorgio and Duarte, 2002; Verdugo et al., 2004; Hopkinson

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

416 417 417 418 418 420 420 422 422 422 422 422 423 423 423 425 425 425 425 426

and Vallino, 2005), interactions with aquatic organisms (Simon et al., 2002; Azam and Malfatti, 2007; Mayer et al., 2011), bioavailability of pollutants (Eadie et al., 1992; Eriksson et al., 2004), and oceanic aquatic phenomena such as mucilage events and marine snow (Smith et al., 1992; Giani et al., 2005; Mecozzi et al., 2005). Some exchange pathways such as aggregation can sequester carbon in sediments and facilitate the settling flux of POM in deep lakes and the open oceans (Grossart and Simon, 1998; Simon et al., 2002; Engel et al., 2004; De La Rocha et al., 2008; Passow, 2012; Zielińska et al., 2014), and they also serve bacteria a colonization area and provides nutrition to living organisms (Azam and Malfatti, 2007; Mayer et al., 2011). And the abiotic conversion of micro-DOM to the macro-aggregates is of great ecological importance because it occurs without carbon losses from the water column (Kerner et al., 2003). The carbon flux from the hydrosphere to the atmosphere is also affected by the exchange efficiency of labile DOM from POM in the riverine systems like the Amazonian rivers (Mayorga et al., 2005). The interactions between terrestrial NOM (mainly POM) and aquatic NOM (mainly DOM) are also involved in the dynamic exchange (Schwesig et al., 2003; Remington et al., 2007; Perez et al., 2011). In addition, NOM can also be categorized into humin, fulvic acid, and humic acid according to its behavior, nature, and structure. This categorization is mainly based on NOM solubility as a function of pH, which was reported to affect the photo-reactivity of DOM as well (Timko et al., 2015). In previous review articles, aggregates and their formation mechanisms have been extensively discussed (Passow, 2002; ZimmermannTimm, 2002; Burd and Jackson, 2009) and the roles of organisms have been emphasized (Simon et al., 2002; Azam and Malfatti, 2007). A conceptual model based on the interactions between minerals and OM has also been proposed to explain the exchange pathway via adsorption (Kleber et al., 2007). However, most related studies have focused only on unidirectional processes. Although there have been some studies addressing bidirectional and/or multi-mechanism processes, the major findings have been mostly deduced from indirect supporting data (Wells, 1998; Simon et al., 2002; Hwang et al., 2006; Yoshimura et al., 2010; Helms et al., 2013). We noted that most previous review articles did not delineate a mechanistic and micro-spatial schema for the complex exchange processes to combine all the associated aspects. Despite

W. He et al. / Science of the Total Environment 551–552 (2016) 415–428

the fact that the coexistence of abiotic and biotic factors may exert either antagonistic (Stordal et al., 1996) or synergistic (Schiebel et al., 2014) effects on the exchange between DOM and POM, the review papers only mentioned the roles of the individual influencing factors. Moreover, the DOM-POM exchanges in mathematical models are described from different aspects in an unsystematic fashion (Yamanaka and Tajika, 1997; Engel et al., 2004; Druon et al., 2010; Wang et al., 2013). Taken together, our objectives throughout this review were to (1) suggest a comprehensive and mechanistic schema to fully describe all different forms of the exchange processes with multiple influencing factors involved, and (2) propose a potentially unified model based on exergy theory to describe all the exchanges in the aquatic ecosystems. Although DOM-POM exchanges occur in a number of aquatic environments such as deep oceans and sediment interstitial waters, this review will mainly focus on inland freshwater and coastal ecosystems. 2. Ecosystem-level perspectives Exchanges between DOM and POM in aquatic ecosystems are an attractive research topic because (1) the OM varies dynamically with respect to phase, size, geographic location and time, (2) the mechanisms are often diversified and complicated, and (3) understanding the similarities and the differences of the exchange between various aquatic ecosystems would provide great benefit for constructing a complete global OM cycle model (Table S1 and Figure S1). The horizontal and the vertical variations of DOM-POM exchanges from an ecological perspective are shown in Fig. 1 and Text S1. In ecosystems such as deep lakes, both DOM and POM are produced by degradation of detritus, followed by the production of secondary POM (SPOM) through

417

aggregation of DOM (Chin et al., 1998; Kerner et al., 2003). During the settling process of larger sized POM, microorganisms selectively degrade the POM, resulting in the depth-dependent variability of POM composition and the preferential production of DOM from POM (Smith et al., 1992; Hwang and Druffel, 2003). The POM settled in the sediments supplies more food to benthic organisms, and the preserved POM which escaped mineralization increases carbon sequestration in the sediments (Simon et al., 2002; von Wachenfeldt and Tranvik, 2008; Passow, 2012). In some other ecosystems, minerals operate as pristine materials to form POM by adsorbing DOM (McKnight et al., 1992; Perez et al., 2011). The size of the minerals and their intrinsic properties mostly determine the differences in the extent of the adsorption (Remington et al., 2007; Liang et al., 2011), and more than 90% of DOM are loaded into POM pool and finally carried into open oceans (Varela et al., 2003). In some closed water bodies, a large amount of POM induces an apparent exchange of DOM to POM which ultimately settles to the sediments (Grossart and Simon, 1998). In turbulent rivers and throughput lakes, however, the exchange maintains a dynamic equilibrium in the water phase and some POM in sediment is even transited into the water and carried out to sea (Varela et al., 2003). In this case, light radiation exerts a much weaker influence on the exchange than in stagnant ecosystems. Photo-induced exchange only occurs in the photic zone of water column (Mayer et al., 2006). 3. Conceptual models of exchange mechanisms Conceptual models previously proposed on the exchange of OM between its dissolved and particulate forms fall two general categories

Fig. 1. Ecological perspective of the dynamic exchanges between DOM and POM (Modified from Simon et al. (2002)). In the ecosystem, oceanic, terrestrial limnetic, riverine, glacial, atmospheric sources are the dominant components of the organic matter pool. Human habitation, agriculture, and industry are gradually becoming a critical issue as they are changing the pre-existing carbon balance. DOM-POM exchanges are widely observed from mountains' streams, through deep and shallow lakes, sandy and polluted rivers, and mixing estuaries, to open oceans. In the weak hydrodynamic forcing environments, the aggregates originated from DOM, called as “lake snow” and/or “marine snow”, are larger and easier to settle to the sediment. This condition is also advantageous for photo-induced and organism-involved exchanges. In turbid environments, the formed POM is easy to collide and break into smaller fragments. DOM-POM exchanges are intensified by the continuous input of minerals, resuspension of sediment, and serious algal blooms caused by anthropogenic activities. Exchanges in estuaries and continental shelves are more complicated due to transitions of salinity, hydraulic residence, sedimentary topography, and water penetration.

418

W. He et al. / Science of the Total Environment 551–552 (2016) 415–428

(Jackson and Burd, 1998; Kleber et al., 2007). The first category, often referred to as the “homogeneous mechanism,” has OM constituents as major participants in the processes, whereas some other factors (e.g., Ca2 +) serve as “accelerants” (Chin et al., 1998; Kerner et al., 2003). The second category, the so-called “heterogeneous mechanism,” involves other materials such as minerals and particulate colloids as well as the OM constituents (Liang et al., 2011; Zielińska et al., 2014). However, actual exchanges between DOM and POM almost always involve other ecological elements (e.g., sunlight and organisms) (Mannino and Harvey, 1999; Mayer et al., 2006). The typical participants, DOMs and POMs are shown in Table 1 and Fig. 2, and described in detail in Text S2 of the supplementary materials. The representative mechanisms are illustrated in Table 2 and Fig. 3, and described in detail as follows. 3.1. Aggregation/dissolution The aggregation of OM is a fundamental process in marine ecosystems, facilitating the sedimentation rate of aggregates (Azam and Malfatti, 2007) and maintaining the inventory of ‘semi-labile OM’, which arises from autotrophic production in surface water but is rather resistant to microbial degradation, in the euphotic layer (Gogou and Repeta, 2010). Various kinds of OMs (e.g., humic substances (HS), polysaccharides (PCHO) and some proteins) participate in the DOM-POM exchange through aggregation (Biber et al., 1996; Chin et al., 1998; Myneni et al., 1999; Wetz and Wheeler, 2007; Verdugo and Santschi, 2010). Aggregation increases the size of DOM, creates the broad molecular weight distribution, and influences its final conformation (Reid et al., 1991; Baalousha et al., 2006; Verdugo and Santschi, 2010).

Table 1 Identified major natural organic matter in the DOM-POM exchange mechanisms. Organic matter

Description

Polysaccharides Consist of long chains of (PCHO) monosaccharide units bound together by glycosidic linkages, which forms fibrillar structure. The polymer gel physics has been used to explain self-assemble of PCHO into colloidal nanogels or microgels in hours and into the macrogels like transparent exopolymer particles (TEP) in days. Amino acids, Composed of amine and peptides and carboxylic acid functional proteins (AA) groups. Most AAs are water soluble while phenylalanine has a hydrophobic phenyl group, rendering amphiphilic property to some peptides and proteins. Humic Including humic acid, fulvic substances acid, and humin and consists of (HS) hydrophilic (e.g. hydroxy, carboxyl, and phenolic) and hydrophobic (e.g. aliphatic and phenyl) parts. Compared with PCHO and AAs, the molecule structure of HS is much more complicated and highly uncharacterized. It is suggested that it is supramolecular associations of relatively small molecules by weak dispersive forces. Its properties are still under continuous investigation with the development of advanced analytical methods.

Reference Passow (2000, 2002); Kovac et al. (2004); Verdugo et al. (2004); Wotton (2004); Giani et al. (2005); Cappiello et al. (2007); Schartau et al. (2007); Gao et al. (2012)

Brownian motion, turbulent shear, differential settling, filtration, bubbling surface coagulation, and bridging with divalent cations are considered as the main processes causing the aggregation (Kepkay, 1994; Zimmermann-Timm, 2002). Brownian motion brings about collisions between constituents of DOM, POM, and the solvent, and is responsible for the slow exchange from DOM to POM via perikinetic (i.e., Brownian) coagulation (Stordal et al., 1996). Turbulent shear determines the collision frequency of larger-sized aggregates (N1 μm) via orthokinetic coagulation, resulted from bulk fluid motion such as stirring (Zimmermann-Timm, 2002). Weak shear promotes the growth of POM, but it may lead to the disaggregation of POM when the shear is too strong (Grossart and Simon, 1998; Goldthwait et al., 2005). In the presence of differential settling, the large sized particles scavenge the smaller ones. Filtration operates in the same manner, in which the smaller particles are scavenged by the laminar-moving particles (Kepkay, 1994). The bubble, generated from either sediment or water turbulence, can promote flocculation phenomenon (Gao et al., 2012). DOM may coagulate on the surface of the bubble and form aggregates up to 32 μm (Johnson and Cooke, 1980). Divalent cations enhance the intermolecular affinity among the OMs like gel-like chemicals and HS (Chin et al., 1998; Schwesig et al., 2003; Baalousha et al., 2006). As shown in Fig. 3a, both gel-like and micelle-like DOM have similar aggregation pathways, such as assembly of individual molecules, cross-linking bridge (or chelation) by cations like Ca2+, Mg2+, and Al3+, annealing of various microparticles to becomes bigger (Chin et al., 1998; Wetz and Wheeler, 2007). The micelle-like DOM form spontaneously and the combined hydrophilichydrophobic nature of amphiphiles determines the propensity to these macromolecules to self-organized (Wershaw, 1999; Kerner et al., 2003). Dissolution, similar to disaggregation, has not received as much attention as aggregation (Goldthwait et al., 2005), and is poorly described mathematically (Jackson and Burd, 1998; Burd and Jackson, 2009). This was a concerned factor in some recent studies of photo-induced exchange (Pisani et al., 2011). The daughter aggregates, caused by the solubilization of macroaggregates, have longer residence time, resulting in reduced carbon flux from the surface to the bottom (Goldthwait et al., 2005), while rapidly dissolving DOM is utilized for organisms' respiration (Mayorga et al., 2005). Thus, the dissolution from POM into DOM is considered as an important process in carbon dynamic models (Druon et al., 2010), which follows the pathways of fragmentation, dispersion, and dissociation as shown in Fig. 3a. 3.2. Adsorption/desorption

Smith et al. (1992); Aufdenkampe et al. (2001); Benetoli et al. (2007); McCarthy et al. (2007)

Baalousha et al. (2006); Baigorri et al. (2007); Mao et al. (2007); Claret et al. (2008); Kang and Xing (2008); Hur et al. (2011); Liang et al. (2011); Zielińska et al. (2014); Piccolo (2001)

In rivers and other lotic ecosystems, DOM is transformed to POM by adsorption onto suspended particles (Remington et al., 2007) which controls the quantity and the composition of DOM and POM (McClain et al., 1997). For example, in the Snake River in Colorado (USA), 40% of the DOM is removed from solution by adsorption onto minerals (McKnight et al., 1992). Such mineral-organics interactions are also found in the deep ocean where the minerals can be endogenous from suspended biogenic solids (De La Rocha et al., 2008). The intimate association of DOM with mineral surfaces leads to the decrease of its mobility and bioavailability (Aufdenkampe et al., 2001), affecting its transportation and the sensitivity to degradation (Perez et al., 2011). Physical intermolecular non-covalent forces (e.g. hydrogen bonding and van der Waals forces) and chemical mechanisms (e.g. ligand exchange) are considered to be the main driving factors of adsorption/desorption (Wershaw et al., 1995; Aufdenkampe et al., 2001; Kleber et al., 2007; Hur et al., 2011). However, the processes involved are noticeably heterogeneous, involving minerals, particulate colloids, and OM constituents (Kleber et al., 2007). Carboxylic groups of DOM are almost always involved in the adsorption of DOM on minerals (Tremblay and Gagne, 2009), and they can be multidentately bound with mineral surfaces as indicated by high values of adsorption enthalpies (Wershaw et al.,

W. He et al. / Science of the Total Environment 551–552 (2016) 415–428

419

Fig. 2. Microscale statuses of various types of DOM and POM and their potential exchanges (some are modified from Verdugo et al. (2004)). In aquatic ecosystems, dead bodies, and exudation of organisms are decomposed into detritus, which is also the precursor of OM (DOM and POM). The truly dissolved organic matter (b1 nm), especially amphiphilic substances like amino acids, peptides, fatty acids, and humic substances are adsorbed onto minerals and aggregates to form mineral-organic substances. The fabric polysaccharide and some amphiphilic substances may self-assemble or photo-induced flocculate to form microgels/colloidal nanogels and micelle-like substances, which serve as the precursors of transparent exopolymer particle (TEP) and humin-rich micelle. Further aggregation and adsorption lead to the formation of the POM such as marine/lake snow, suspended solids, and sediments. In the particulate phase, marine/lake snow can be transformed into dissolved forms by bio-/photo-degradation, dissolution, and photo-dissolution, and the organic suspended solids and sediments are transformed mainly through desorption, followed by dissolution, photo-dissolution, or bio-/photo-degradation.

1995). Amphiphilic compounds (e.g. HS and amino acids (AA)) exhibit a variety of adsorption forms due to the presence of both polar and nonpolar structures (Kleber et al., 2007). For example, the hydrophilic fractions of HS can be adsorbed on minerals via electrostatic forces and/or ligand exchange reactions (Kang and Xing, 2008), while the hydrophobic fractions are absorbed via hydrophobic interactions (Hur et al., 2011). Hence, higher molecular weight DOM with more aromatic, carboxyl, and hydrophobic fractions tends to be more highly adsorbed on minerals (i.e., preferential adsorption) (Aufdenkampe et al., 2001), and the exchange would be apparently irreversible due to the formation of highly stable mineral-organic multidentate surface complexes (Wershaw et al., 1995; Jagadamma et al., 2012). The positively charged groups on AA are capable of electrostatic interactions with aluminosilicates, which have net electronegative charges at natural pH (Aufdenkampe et al., 2001; Benetoli et al., 2007). Kleber et al. (2007) have proposed a conceptual model of mineral-organic interaction as shown in Fig. 3b (Kleber et al., 2007). This model successfully explained various adsorption behaviors between DOM and minerals. Briefly, the mechanism depends on conformation of the three various zones,

which are the low charged smectite-like minerals with protein-like substances, the smectite-like minerals with hydrous iron oxide, and the kaolinite-like minerals without charge (Fig. 3b). In the first internal zone, namely, contact zone, three typical chemicals (hydrous iron oxide, amphiphilic protein-like chemicals, and hydrophobic chemicals) are coated on the electronegtively charged surfaces or uncharged minerals via electrostatic interaction and/or hydrophobic interaction. The surface of the contact zone includes polar and nonpolar functional groups. Amphiphilic chemicals are also associated with them via electrostatic interaction and hydrophobic interaction. The polar parts of these amphiphilics constitute the hydrophobic interaction zone, in which other amphiphilic and hydrophobic chemicals might be absorbed. This zone does not exist continuously because the coated protein-like chemicals can directly interact with the molecules in the kinetic zone. In the outer region, the interaction is governed by hydrogen bond, multivalent cations, and electrostatic forces. It is noteworthy that this model has been developed for soils. In other ecosystems, many conditions, including the conformation and the charges of OM as well as the mineral surface, could be changed.

420

W. He et al. / Science of the Total Environment 551–552 (2016) 415–428

Table 2 Exchange mechanisms between DOM and POM summarized from Table S1. Direction Exchange mechanisms

Abiotic Driving factors or biotic

Reference

DOM →

Aggregation, coagulation

Abiotic Brownian motion, turbulent shear, differential settling, filtration, and bridging with divalent cations

Adsorption

Abiotic The physical intermolecular weak forces (e.g. hydrogen bond and van der Waals force) and chemical mechanisms(e.g. ligand exchange)

Dissolution

Abiotic The reversible process of aggregation

Desorption

Abiotic The reversible process of adsorption

Photo-dissolution

Abiotic Photo-oxidation of POM

Biodegradation

Biotic

Aggregation and solubilization Aggregation and microorganism decomposition Adsorption and desorption Adsorption and plankton decomposition

Abiotic Mentioned in aggregation/dissolution

Reid et al. (1991); Stordal et al. (1996); VanHeemst et al. (1996); Chin et al. (1998); Passow (2000, 2012); Kerner et al. (2003); Schwesig et al. (2003); Engel et al. (2004, 2014); Thornton (2004); Bhaskar et al. (2005); Giani et al. (2005); Baalousha et al. (2006); Baigorri et al. (2007); Mari et al. (2007); Wetz and Wheeler (2007); von Wachenfeldt and Tranvik (2008); Gogou and Repeta (2010); Asmala et al. (2014); Shiu et al. (2014) Druffel and Williams (1990); McKnight et al. (1992); Wershaw et al. (1995); Aufdenkampe et al. (2001); Kaiser et al. (2001); Hwang and Druffel (2003); Pullin et al. (2004); Remington et al. (2007); Wetz and Wheeler (2007); Kang and Xing (2008); von Wachenfeldt and Tranvik (2008); Perez et al. (2011); Pisani et al. (2011); Gao et al. (2012); Jagadamma et al. (2012); Passow (2012); Zielińska et al. (2014) Pullin et al. (2004); Druon et al. (2010); Helms et al. (2013); Chen et al. (2014) Komada and Reimers (2001); Goldthwait et al. (2005); Osborne et al. (2007); Pisani et al. (2011) Koelmans and Prevo (2003); Mayorga et al. (2005); Swan et al. (2009) Kieber et al. (2006); Mayer et al. (2009, 2011); Estapa and Mayer (2010); Shank et al. (2011); Southwell et al. (2011); Helms et al. (2014); Schiebel et al. (2014); Yang et al. (2014) Moran and Buesseler (1992); Smith et al. (1992); Lara and Thomas (1995); Mannino and Harvey (1999); Wetz et al. (2008) Sannigrahi et al. (2006)

Both

Kovac et al. (2004); Mecozzi et al. (2005); Le Moigne et al. (2013)

POM

Photo-flocculation/adsorption Abiotic Photo-oxidation of DOM POM → DOM

DOM ↔ POM

Supply and depletion of the OM

Mentioned in aggregation/dissolution and organisms-involved exchange

Abiotic Mentioned in adsorption/desorption Both Mentioned in adsorption/desorption and organisms-involved exchange

As the reversible process of adsorption, desorption might cause the mobilization of up to 100% of indigenous POM from the suspended solids and resuspended sediments (Komada and Reimers, 2001; Koelmans and Prevo, 2003; Osburn et al., 2012), which is important for climate change since the carbon flux from immobile phase like sedimentary POM pool might results in potential augmentation of CO2 via organisms' respiration (del Giorgio and Duarte, 2002; Azam and Malfatti, 2007). To account for the heterogeneous property of OM mixture, modified Langmuir isotherm models have been employed to describe the adsorption/desorption behavior of DOM on minerals (Gu et al., 1994; van de Weerd et al., 1999), and strong hysteresis is typically observed. 3.3. Photo-induced exchange The penetration of light through the water column can impact DOMPOM distributions in some (e.g., non-turbid) aquatic ecosystems (Table 2). For example, DOM constituents released from settling POM may be relatively recalcitrant until being degraded by solar bleaching, which is an important pathway of carbon flux from the hydrosphere to atmosphere (Swan et al., 2009). In recent years, many related phenomena such as photo-flocculation of colored DOM, photo-dissolution of the detritus from organisms, photo-adsorption of DOM, and photodesorption of suspended solids and resuspended sediment have been investigated through artificial microcosm experiments (Kieber et al., 2006; Mayer et al., 2006, 2009; Hur et al., 2011; Helms et al., 2013). Such DOM-POM exchanges often occur at rates much faster than those without light (Schiebel et al., 2014). In most cases, photoinduced exchange result from the photo-oxidation of DOM and POM which may subsequently alter previous interactions and/or distributions between DOM and POM driven by aggregation/dissolution and/ or adsorption/desorption (Fig. 3c) (Gao and Zepp, 1998). The pigments,

Benetoli et al. (2007); Liang et al. (2011) Grossart and Simon (1998); Hwang et al. (2006)

unsaturated lipids, humic acid, and tryptophan in OM have been shown to be participants in the production of reactive oxygen species (ROS) in the presence of light (Mayer et al., 2009; Cottrell et al., 2013). Photoirradiation can degrade some larger DOM constituents into intermediate sizes which are more easily adsorbed on minerals (Pullin et al., 2004). Therefore, the two processes together promote the exchange of POM from DOM, producing a lower molecular weight, less aromatic DOM pool than either individual process by itself (Pullin et al., 2004). Photo-oxidation typically adds more oxygen-containing functional groups to the POM, which generally increases the polarity and thereby enhances the water solubility of OM in the aggregates (Estapa and Mayer, 2010). The humic-like OM, originated from both terrestrial humics and humified algal DOM (Helms et al., 2014), are released to a greater extent from sediment POM than protein-like OM via photodissolution and/or photo-desorption (Shank et al., 2011). Although photo-induced exchanges are expected to be irreversible because of the oxidation-driven destructive changes in the original OM molecules (Estapa and Mayer, 2010; Chen et al., 2014) and other elimination mechanisms like the complete degradation into inorganic matter (CO2) (Yang et al., 2014), the altered OMs can also participate in the exchange mechanism through adsorption/desorption or aggregation/dissolution as shown in Fig. 3c (Mayer et al., 2006; Pisani et al., 2011; Porcal et al., 2013), which can be viewed as an apparent reversible exchange between DOM and POM. 3.4. Organism-involved exchange Organisms are always involved in abiotic exchanges via the supply and depletion of OM (Smith et al., 1992; Wetzel, 1995). They supply OM through excrement and/or secretion with their dead bodies as well (Simon et al., 2002; Wetz et al., 2008). Based on the ballast hypothesis, fluxed of POM to the deep sea may be determined by the flux of

W. He et al. / Science of the Total Environment 551–552 (2016) 415–428

421

Fig. 3. Schemas of mutual DOM-POM exchange pathways (charts a and b are modified from Chin et al. (1998) and Kleber et al. (2007), respectively). The exchange pathways between DOM and POM can be summarized as two fundamentally reversible abotic mechanisms — aggregation/dissolution (a) and adsorption/desorption (b). In the former, there are three pathways (assembly, chelation, and annealing) for the gel-like (e.g. polysaccharide) and micelle-like (e.g. amphiphilics) DOM to form POM. The reversible pathways are dispersion, dissociation, and fragmentation. According to the organo-mineral interaction models (Kleber et al., 2007), the adsorption/desorption mechanism is not only a simple attaching process with mineral surfaces. The processes take place in the three regions consisting of contact zone, zone of hydrophobic interactions, and kinetic zone (outer zone). Sunlight and aquatic organisms are often involved, making the exchange mechanisms more complicated (i.e., photo-induced (c) and organisms-involved DOM-POM exchanges (d)). Ultraviolet dominates the photo-oxidation by producing reactive oxygen species (ROS). After degradation of the labile chemicals in POM and DOM, refractory organic matter (ROM) as a new pool, influences the pre-existing balance between POM and DOM. Organisms, especially bacteria, produce various extracellular enzymes like hydrolase and oxidase, which participate in the decomposition of various OM.

minerals and that calcium carbonate is an efficient “carrier” of POM (Armstrong et al., 2002). However, The mineral part of detritus (e.g., silica diatom frustules) also offers a carrier for adsorption of DOM and no evidence shows that calcium carbonate has a higher carrying capacity of OM than biogenic silica in the previous study (De La Rocha et al., 2008). Depletion mechanisms are more complicated because different types of organisms have their own depletion pathways. Simply, high level trophic animals simultaneously consume both DOM and POM via ingestion, while unicellular organisms like bacteria and protozoa ingest only smaller-sized OM (Wetzel, 1995; Simon et al., 2002).The primary depletion and the supply mechanisms generate notable changes in the quantities of DOM and POM pools, resulting in a perturbation of the existing balances (Skoog and Benner, 1997). On the other hand, the secondary depletion mechanism primarily changes the properties of the OM, leaving refractory organic matter (ROM) by selective biodegradation of labile OMs and further by microbial humification (Mannino and Harvey, 1999; Loh et al., 2008). That mechanism is also proposed as microbial carbon pump, which is a conceptual framework for understanding the role of microbial processes in the production of ROM (Jiao et al., 2010; Lechtenfeld et al., 2015). Three pathways were identified:

1) direct exudation of microbial cells during production and proliferation, 2) virallysis of microbial cells to release microbial cell wall and cell surface macromolecules, and 3) POM degradation (Jiao et al., 2010). The second depletion may be directly involved in abiotic exchanges as described above, sometimes making the exchange between DOM and POM irreversible (Wetz et al., 2008). For aggregates highly colonized by bacteria (e.g., “marine snow”), hydrolytic enzymes can transform POM into non-settling DOM (Smith et al., 1992; Wells, 1998), creating plumes in the opposite direction of settling (Azam and Malfatti, 2007) and the vertical variability of fluorescent matter (Bushaw et al., 1996). Some labile DOMs such as dissolved protein-like substances and lipids are further biodegraded and completely mineralized into inorganic matter (VanHeemst et al., 1996; Mannino and Harvey, 1999; Gogou and Repeta, 2010), while humic-like substances may result in self-assembly/gel-like particles or adsorb on minerals (Kerner et al., 2003; Zielińska et al., 2014). With regard to mineral-organic substances (MOS), microorganisms can interfere with DOM adsorption by colonizing mineral surfaces or promoting DOM assimilation (Aufdenkampe et al., 2001; Yoshimura et al., 2010). Organisms-involved exchange, as shown in Fig. 3d, is similar to lightinduced exchange. However, the former is much more complicated

422

W. He et al. / Science of the Total Environment 551–552 (2016) 415–428

because of the diversities of organism activities, including ingestion, biosynthesis, biodegradation, and colonization on the adsorbent. 4. Main influencing factors Factors influencing DOM-POM exchange, as shown in Fig. 4, have been selected based on critical reviews of recently published literature in Table S1, and are ranked in Figure S2. Among these factors, the properties of DOM and POM, light, ions, and organisms are the most extensively examined in the literature. The details are described in the following text. 4.1. Physico-chemical factors 4.1.1. Properties of organic matters The sources or chemical composition of OM affect the exchange behavior of DOM in indirect ways (Loh et al., 2008; von Wachenfeldt and Tranvik, 2008; Gogou and Repeta, 2010; Porcal et al., 2013), and the exchange direction is determined by the DOM concentration. For example, increased polysaccharide amounts promote the formation of transparent exopolymer particles (TEP) (Engel et al., 2004), and a high level of POM may disaggregate to release DOM in the deep sea (Verdugo et al., 2004). The concentration of POM precursors, the stickiness of particle surface, the velocities, and the probability of attachment are all involved in controlling aggregation and settling (Zimmermann-Timm, 2002). Carbonaceous particles have negative effects on the formation of POM, hindering the cross-linking bridges between microgel and Ca2+ and reducing the equilibrium sizes (Shiu et al., 2014). Aggregation largely depends on the initial sizes of DOM (Gao et al., 2012). For example, largersized DOM molecules, such as polysaccharides, aggregate more easily than smaller ones (e.g., oligosaccharides) (Verdugo and Santschi, 2010; Gao et al., 2012). The stability of MOS is influenced by mineral properties such as surface charge, porosity, chemical structure, and specific surface area (Komada and Reimers, 2001; Kleber et al., 2007). Mineral-containing aggregates can grow more quickly and larger due to the additional adsorption of DOM (Le Moigne et al., 2013).

Fig. 4. Factors influencing DOM-POM exchanges. Based on the previous reports published in the past two decades, seventeen elements are identified to involve in exchanges, including the chemical composition of DOM and POM and abiotic and biotic factors. The size of the circle and number in each bracket represents the number of relevant publications from SI Table 1. Phytoplankton is the most important factor in the biotic factors, followed by bacteria, while sunlight is the most frequently highlighted as an important abiotic factor in recent years, followed by hydrodynamics, temperature, pH, cations, and mineral properties. Some other factors, such as zooplankton, macrophyte, season, salinity, nutrients, and carbon dioxide, are also concerned in various aquatic ecosystems or microcosms.

4.1.2. Light, temperature, and redox environment The degree of photo-induced exchange is affected by the energy, exposure duration, and light intensity (Schiebel et al., 2014). The photoflocculation of DOM occurs during the early stages of light exposure (Chen et al., 2014). Moreover, light may be sharply attenuated in most freshwater bodies (excluding ultra-oligotrophic water bodies) due to a high level of DOM (Schindler and Curtis, 1997). The intensity of the short-wavelength light notably decreases with depth in the open sea, reducing the photo-induced exchange (Determann et al., 1996; Mayer et al., 2006). The mechanisms of photo-release of DOM from POM differ by the wavelength of light. For UV light, the high energy may result in the production of ROSs which further decompose POM into small molecular DOM or even inorganic matter (Gao and Zepp, 1998). Although infrared light cannot produce ROSs directly, it stimulates the release of OM from POM via the warming effect from increased motion and vibration of chemical molecules. Increasing temperature might influence the release of OM from POM. In this case, hydrophilic OM is more sensitive than hydrophobic OM (Kaiser et al., 2001). Kerner et al. (2003) have claimed that the abiotic aggregation from DOM to POM would depend solely on the temperature and capacity of aggregated DOM (Kerner et al., 2003). Meanwhile, the reversible dissolution is enhanced by increasing temperature (Mayer et al., 2006). Nevertheless, a higher temperature can enhance bacterial activity and the generation of DOM and POM. Furthermore, POM, which should have settled into the sediment, might be converted to DOM and further to CO2 via organismsinvolved exchange (Thornton, 2004; Ma et al., 2014). In the reductive environment like sediment-water interface, reductive dissolution of mineral oxides (FeOOH coated on the sediment surface) might cause the release of DOM from POM by adsorption/desorption mechanisms (Skoog et al., 1996). Oxygen enhances photo-induced exchange through the production of ROSs such as singlet oxygen (Mayer et al., 2009). The carbon dioxide produced by mineralization of OM can feed back and enhance the organisms-involved exchange (Engel et al., 2014). 4.1.3. Ions (multivalent cations, pH, total alkalinity, inorganic nutrients, and salinity) Multivalent cations are involved in both aggregation/dissolution and adsorption/desorption. Numerous studies have evidenced the enhanced aggregation effects of the common multivalent cations (e.g., Ca2 +) through cross-linking bridges (or chelation) (Chin et al., 1998; Passow, 2000; Engel et al., 2004; Baalousha et al., 2006; Mari et al., 2007; Shiu et al., 2014). Aluminum (Al3+) and iron ions (Fe2+, Fe3+) easily flocculate into hydrous oxides coating on minerals and facilitate the formation of POM (McKnight et al., 1992; Schwesig et al., 2003). Those multivalent cations are also important factors that form the organic multilayer through bridging interaction between DOM and organic matters attached on minerals (Kleber et al., 2007). Flocculation of DOM in the presence of cations like Fe3+ and Al3+ during the mixing of river water and seawater was previously reported (Sholkovitz, 1976; Sholkovitz et al., 1978). In the photo-induced exchange, iron (Fe3+ and Fe(OH)3) is found to co-flocculate with DOM to form POM via aggregation (Helms et al., 2013; Chen et al., 2014). Thus, POM and some metals are often coupled in DOM-POM exchange, contributing to the transfer of DOM and metals to sediments in aquatic systems (Porcal et al., 2013). It was also observed that further photolysis of DOM might result in the reduction of the metals (e.g., Fe3 + to Fe2 +) causing disaggregation (Voelker et al., 1997). The phenol and hydroxyl groups of OM such as humic substances are weakly dissociated at low pH, making the OM remain more in the form of particles (Baalousha et al., 2006; Baigorri et al., 2007). In detail, H+ would enhance the aggregation of organic matter through the generation of more H-bonds among carboxylic and/or phenolic acidic groups of organic matter (Alvarez-Puebla and Garrido, 2005). The H+ tends to decrease the surface charge of minerals and enhance the protonation of acidic functional groups of organic matter, resulting in reduction of the net electrostatic repulsion between DOM and minerals and also

W. He et al. / Science of the Total Environment 551–552 (2016) 415–428

the stabilization of hydrophobic interactions between DOM and organic matters attached on minerals (Pullin et al., 2004; Benetoli et al., 2007; Liang et al., 2011; Perez et al., 2011). Both of the two processes would benefit the DOM-POM exchange driven by adsorption mechanisms. Meanwhile, deprotonated functional groups and the subsequent increase of electrostatic repulsion may present a barrier to the OM exchange from a dissolved phase to a particulate phase at neutral pH (Pullin et al., 2004; Liang et al., 2011). The total alkalinity (OH– and CO2– 3 ) also influences the formation of TEP, but the molecular structures regulating abiotic TEP formation are not well understood at present (Passow, 2012). The nutrients (e.g. carbohydrate and phosphorus) can influence the organisms-involved exchange via enhancement of microbial activity (Thornton, 2004; Azam and Malfatti, 2007; Yoshimura et al., 2010). Little to no impact of salinity on the photo-dissolution of POM is reported (Mayer et al., 2006). Because salinity has little effect on the production of ROS (Sandvik et al., 2000), it can be deduced that some functional groups of OM susceptive to the salinity might be inactivated or altered via photochemistry. 4.1.4. Hydrodynamic factors While all the factors above are internally involved in the DOM-POM exchanges as micro indicators, hydrodynamic factors, including river discharge (Agatova et al., 1996), estuarine plume process (Dagg et al., 2004), water turbulence (Alldredge et al., 2002), resuspension effect (Koelmans and Prevo, 2003), water residence time (Mari et al., 2007), and water depth (Hwang and Druffel, 2003), operate apparently and externally as macro indicators. For example, POM was increased by oil output in Sakhalin shelf, while a river discharge promoted an increase of DOM in the Sakhalin Bay, indicating various DOM-POM exchanges in different water layers (Agatova et al., 1996). POM and some highmolecular-weight DOM may partition into a lower layer, quickly settle down to sediments, and finally be lost from plume water. Moreover, rapid exchanges between DOM and POM (e.g., aggregation, flocculation, and desorption) also occur in a low salinity condition or near-field portion of plume. Such physical and optical changes due to plume process may also increase phytoplankton production of DOM from inorganic nutrients and simulate the activities of organisms because of the release of riverine DOM through photochemical and microbial processes (Dagg et al., 2004). Strong water turbulence interferes with the growth of macroaggregates (Simon et al., 2002) whereas the low turbulence favors it (Mecozzi et al., 2005), which indirectly affect the organism-involved exchanges. Resuspension, caused by wind or fish, or during dredging, may bring turbulence effect on POM in the interface between water and sediments, further affecting the OM partition between the POM and the DOM pools (Koelmans and Prevo, 2003). Long water residence time prolongs the bacterial degradation of DOM (Mari et al., 2007). Water depth affects the exchanges because of its vertical variations of light, organisms, water turbulent, temperature, and salinity (Determann et al., 1996; Skoog and Benner, 1997; Loh et al., 2008; von Wachenfeldt and Tranvik, 2008).

423

bacteria (e.g., Pseudomonas mendocina var.) can dissolute the minerals like Al-substituted goethite at sediment-water interface, releasing DOM to the overlying water (Maurice et al., 2000). Zooplankton participates in changing the bacterio- and phytoplankton (e.g. diatom) community by grazing, which indirectly influences the DOM-POM exchanges (Druon et al., 2010). The proteinaceous material such as AA in the sinking POM often has a main source from zooplankton (McCarthy et al., 2007). The structure of macrophyte community determines the quality and quantity of the derived OM because various species contribute to DOM differently in the characteristics. For example, it was reported that nine different senescent plants produced the biomass with dissimilar fiber fractions, carbon contents, and molecular weight distributions, finally responsible for the diversity of produced labile DOM from POM (Osborne et al., 2007). 5. DOM-POM exchanges in mathematical models Besides several conceptual models to illustrate DOM-POM exchanges in aquatic ecosystems (Simon et al., 2002; Azam and Malfatti, 2007; Kleber et al., 2007), many mathematical models have been considered to describe the phenomena on the global, or the regional, or the microcosmic scale (Yamanaka and Tajika, 1997; Engel et al., 2004; Druon et al., 2010; Wang et al., 2013) (Table 3). Typically, the DOMPOM exchange is posed as only a small component of most global or regional scale models, and its exchange mechanism is unclear. In the models, the concentrations of POM or DOM are estimated using the production yields of other model components (e.g. sediment, soil and organisms) based on mass balance. Although some regional models addressed aggregation/dissolution, photo-induced and organismsinvolved exchange processes as well as various influencing factors (Druon et al., 2010; Mukherjee et al., 2013). The complexity of DOMPOM exchange in microcosmic scale has been often overlooked, which is affected by many influencing factors (Table 3). Therefore, we paid special attention on the mathematic models to describe the major individual DOM-POM exchange mechanisms first. To date, aggregation/dissolution, adsorption/desorption, photo-induced, and organismsinvolved models have been successfully described by PCHO-TEP dynamic model (Engel et al., 2004), dynamic adsorption/desorption model (van de Weerd et al., 1999), photochemical transformation model (Porcal et al., 2013), and microbial-enzyme-mediated decomposition model (Wang et al., 2013), respectively. Since the aforementioned mathematical models focus the individual mechanisms of DOM-POM exchanges, it is beneficial to establish a unified model to conceptually combine all the major mechanisms and fully address the DOM-POM exchange behavior. In this context, available energy, namely exergy, (unit, kJ) is suggested as a good unifying property because it drives all the mechanisms associated with DOM-POM exchanges (Dewulf et al., 2008). In the abiotic reaction (e.g. aggregation/ dissolution, adsorption/desorption, and photochemistry), for example, the physical exergy (Exph, kJ per unit mass) and chemical exergy (Ex0ch,i, kJ) can be expressed by Eqs. (1) and (2), respectively:

4.2. Biotic factors Exph ¼ ðh–T 0 sÞ–ðh0 –T 0 s0 Þ ¼ u þ P 0 v–T 0 s0 –g0 Bacteria and phytoplankton are the most important factors, followed by zooplankton and macrophyte (Fig. 4). Bacteria also have a significant influence on the photo-released of DOM from POM though ingestion or exudation. In detail, the actual DOM amount reflects the net quantity of the observed DOM and the DOM ingested or exudated by bacteria (Mayer et al., 2009; Jagadamma et al., 2012; Schiebel et al., 2014). Bacterial and phytoplankton (e.g. diatom) community may have different growth efficiencies and different degradation abilities, which also influence the exchange rates of DOM-POM exchange (Verdugo et al., 2004; Bhaskar et al., 2005; Mari et al., 2007; Wetz and Wheeler, 2007). For instance, bacteria- and phytoplankton-produced EPS can be transformed into different forms of TEP, and the final size of POM is much larger for the diatom versus the bacteria (Bhaskar et al., 2005). Some aerobic

Ex0 ch;i ¼ ΔG0 r þ

X

v Ex0 ch;k k k

ð1Þ ð2Þ

where h and s are the enthalpy and the entropy of the system, h0, s0, and g0 are the enthalpy, entropy, and Gibbs free energy (each per unit mass) at the standard “environmental” temperature (T0, usually 298.15 K) and pressure (P0, usually 101,325 Pa), respectively, and ΔG0r, vk, and Ex0ch,k are the standard Gibbs energy of the reference reaction, the number of moles and the standard chemical exergy (kJ/mol) of the kth reference species, respectively. The property of exergy has also been successfully used in the organism component of ecological models, reflecting both organic matter and

424

W. He et al. / Science of the Total Environment 551–552 (2016) 415–428

Table 3 Mathematical models of DOM-POM exchanges. Model name Global scale models Carbon cycle model (BMR) Ocean biogeochemical general circulation model Global Nutrient Export from Watersheds (NEWS) models

Brief description

Exchange direction and mechanism

Influencing factors

References

Based on an oceanic general circulation model and improved by considering both DOM and POM Including horizontal and vertical OM flux and production and consumption processes of DOM in ocean Estimating the export globally as a function of land use, nutrient inputs, hydrology, and other factors

Unclear

Non-specific

Bacastow and Maier-Reimer (1991) Yamanaka and Tajika (1997) Seitzinger et al. (2005)

Eatherall et al. (1998)

Regional scale models Carbon flux model

Used in estuary based on mass balance and DOM and POM production rate by various media Organic matter (OM) Used in head stream based on mass balance and DOM dynamics model and POM determined in situ The three-dimensional ocean Widely used for shelf circulation and coupled circulation model (ROMS v3) physical-biological applications Time-based isotope Estimating temporal source contributions to POM and mixing model DOM in watershed based on mass balance of isotope Carbon dynamics model Containing carbon in 7 statuses and many physical, chemical, biological components and processes Microcosmic scale models DOM released by sediment suspensions equation PCHO-TEP dynamic model

Phytoplankton DOM release and death model Coagulation equation Dynamic adsorption/ desorption model Photochemical transformation model Microbial-enzyme-mediated decomposition model

POM → DOM A, D Unclear

E

I-1, II-1, III-2, III-8, III-9, IV-1, IV-2, IV-3 Non-specific

Unclear

E

Non-specific

POM → DOM D, E

I-3, II-1, II-3, III-4, IV-1, IV-4 Karlsson et al. (2005)

DOM ↔ POM A, C, D III-1, III-2, III-5, III-8, III-9, IV-1, IV-2, IV-3, Unclear E Non-specific

Produced by incomplete mineralization of POM or by desorption from mineral surfaces Based on the concept that acidic polysaccharides approaching each other by diffusion can adhere and Smoluchowski equations Estimating the DOM produced by POM derived from phytoplankton on the basis of carbon and nitrogen Estimating the rate of change of the particle size spectrum in a well-mixed layer as well as POM's distribution Based on pseudo-first-order and pseudo-second-order models, Langmuir model and improved by considering competition Described by the kinetics of pseudo consecutive reactions Including particulate, mineral-associated, dissolved organic matter, microbial biomass, and associated exoenzymes based on the Michaelis-Menten kinetics in soil system

E

Druon et al. (2010) Hossler and Bauer (2012)

DOM ↔ POM A, C, D I-3, II-1, II-3, III-1, III-5, III-10, IV-2

Mukherjee et al. (2013)

POM → DOM B

II-1, II-3, III-2

Koelmans and Prevo (2003)

DOM → POM A, D

I-1, I-2, I-3, II-2, II-3, III-3, III-5, IV-1

Engel et al. (2004); Schartau et al. (2007)

POM → DOM D

I-1, I-2, II-3, IV-1

Flynn et al. (2008)

DOM → POM A

I-1, II-3, III-2, IV-1

Burd and Jackson (2009)

DOM → POM B

I-1, I-2, I-3, II-3, III-3, III-4, III-5, III-6

van de Weerd et al. (1999); Liang et al. (2011)

DOM ↔ POM C, D

III-1, III-3, III-4, III-7, IV-2

Porcal et al. (2013)

DOM ↔ POM B, D

I-3, II-3, III-10, IV-2

Wang et al. (2013)

Note: A. aggregation/dissolution, B. adsorption/desorption, C. photo-induced exchange, D. organism-involved exchange, E. empirical estimation on basis of mass balance; I-1. DOM-chemical composition, I-2. DOM-molecular weight, I-3. DOM-concentration, II-1. POM-sources, II-2. POM-size, II-3. POM-concentration, III-1. light, III-2. hydrodynamics, III-3. cations, III-4. pH, III-5. temperature, III-6. mineral, III-7 season, III-8. salinity, III-9. inorganic nutrients, III-10. CO2/O2, IV-1. phytoplankton, IV-2. bacteria, IV-3. zooplankton, IV-4. macrophyte.

taxa (Jørgensen, 1992; Jørgensen and Svirezhev, 2004). The biological exergy (Exbio, kJ) is calculated by the probability of producing organic matter and the probability of finding the corresponding genetic code (Pq) as shown in the Eq. (3). The former term refers to the classical exergy, which denotes the capacity of OM production, and the latter is the informational exergy expressed based on the DNA information of the involved organisms. X  X   Exbio ¼ ðμ 1 –μ 1 eq Þ p cp –RT 0 q cq ln P q ;

ð3Þ

ðp ¼ f1; 2; 3; …; Ng; q ¼ f2; 3; 4; …; NgÞ where (μ1 − μeq 1 ) is the specific free energy of detritus as indicated by the difference between the chemical potential of organic matter at an actual environment condition (μ1) and the thermodynamic equilibrium (μeq 1 ), cp and cq are the concentrations of the pth or qth component (gram), respectively, N is the number of components or organisms (taxa) in the ecosystem, and R and T0 are the gas constant (8.314 J K−1 mol−1) and environmental temperature (K), respectively. In a relevant reference (Debeljak, 2002), Pq was expressed as 20−700g where 20 is the amount of essential amino acids used in proteins of living organisms, g is the amount of genes in species q, and 700 is the average amount of encoded amino acids in a gene. However, the constant 700 was a rather rough approximation of encoded amino acids in a gene due to the lack of the data on the amount of genes and the occurrence of nonsense DNA (Debeljak, 2002). More recent calculation was based on

the nucleotides information and the parameter was expressed as 4−aq(1 − gq) where 4 is the amount of coding amino-acids in living organism, aq is the amount of nucleotides in the genome, and gq the percentage of repeating genes (Susani et al., 2006). We combined both the biotic and the abiotic reactions to propose a unified conceptual mechanism based on exergy theory as shown in Fig. 5. If we assume that DOM-POM systems should approach the status of dynamic equilibrium, all the exchange reactions would be driven by the exergy components (Ex1, Ex2, Ex3, and Ex4). In this case, all the influencing factors can be added to the conceptual model because they are also governed by various types of exergy. The proposed model includes three fundamental components, which are total exergy driving the DOM-POM exchange (Extot, Eq. (4)), the total exchanged OMs (OMtot, Eq. (5)), and the exergy efficiency of various exchange mechanisms (EEFw, Eq. (6)). Extot ¼ ¼

X Xw

OMtot ¼

w

Exw þ Exother þ Exif þ Exwaste OM w  EE F w þ Exother þ Exif þ Exwaste

X w

OM w

EE F w ¼ U w ð f 1 ; f 2 ; f 3 ; …; f n ; Exif Þ

ð4Þ ð5Þ ð6Þ

where Extot includes the exergy used for DOM-POM exchange by various mechanisms (ΣwExw), the exergy used for other pending

W. He et al. / Science of the Total Environment 551–552 (2016) 415–428

components (Exother), the exergy to drive the influencing factors (Exif), and unused exergy (Exwaste). A certain fraction of the total exchanged OM (OMw) involves a particular mechanism with EEFw, in which various influencing factors (f1, f2, f3, …, fn) are involved and the corresponding exergy (Exif) is operated under a certain unidentified function (Uw). This conceptual model is promising in that DOM-POM exchanges can be described in a unified way. However, the degree of the exergy efficiency involving various exchange mechanisms should be further examined and validated by the laboratory or field data. Furthermore, more knowledge is required for mathematical complement and should be incorporated into the current forms in the future. 6. Summary and future prospects DOM-POM exchanges have been explored in numerous studies, but little systematic effort has been made to summarize the complicated phenomenon with attention on the influencing factors from both macro-(ecological) and micro-(molecular) level perspectives. In addition, many aspects still remain unanswered concerning the roles of the organism's community. Concrete evidence is needed on the mutual DOM-POM exchanges and effects of anthropogenic activities. All things taken together, future studies should be focused on the topics concerning (1) coupling field observations with elaborately designed experiments, (2) employing more advanced analytical methods, and (3) the improvement of proposed unified DOM-POM exchange models. The DOM-POM exchange using the data from field investigation might reflect natural conditions better than lab simulation experiments. Nevertheless, lab experiments have been extensively conducted because it can offer clearer explanations of the individual transformations. Coupling field observation with elaborately designed experiments might provide the key routes for answering many unexplored issues. The DOM-POM exchange is posed as only a small component of most global or regional scale models, and its exchange mechanism is unclear. Since the aforementioned mathematical models focus the individual mechanisms of DOM-POM exchanges, it is beneficial to establish a unified model to conceptually combine all the major mechanisms and fully address the DOM-POM exchange behavior. Analytical chemists still seek improved analytical protocols to obtain more information about both DOM and POM to clarify DOM-POM

425

exchange mechanisms, although a number of analytical methods are available for DOM-POM exchanges studies (Fig. 6). However, some drawbacks have been pointed out. For example, exchange process like aggregation may be mistakenly understood due to the diversity of the factual environmental particles, which could not be simply interpreted by one aggregation model (Jackson and Burd, 1998). Depending on mature microphotography methods and spectrophotometric methods, we are more familiar with some microparticles like TEP. Nevertheless, the techniques are semi-quantitative and the relative chemical composition of microparticles is still unknown (Verdugo et al., 2004). Many field investigators have traced DOM-POM exchanges using radiolabel 14C and elemental analysis based on some simple and limited assumptions (Hwang and Druffel, 2003; Hopkinson and Vallino, 2005). The ultrahigh resolution mass spectrometry, Fourier transform ion cyclotron resonance mass spectrometry, has been employed to pinpoint exact compositions of OM and its functional groups recently (Hertkorn et al., 2013). However, it still can only offer semi-quantitative information (Helms et al., 2013; Chen et al., 2014). A conceptual model based on exergy theory is proposed such that DOM-POM exchanges can be fully described in a unified way and all influencing factors can be taken into account. However, more knowledge is warranted for mathematical complement, which should be incorporated into the current forms. Acknowledgments This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIP) (No. 2014R1A2A2A09049496). Appendix A. Supplementary data Supplementary materials in this study include case studies of the exchanges between DOM and POM and statistical analysis of dominated process, exchange direction, data source, influencing factors, and matrix. This information is available free of charge via the internet at http://www.sciencedirect.com/ Supplementary data associated with this article can be found in the online version, at http://dx.doi.org/10. 1016/j.scitotenv.2016.02.031.

Fig. 5. A hypothesized conceptual schema of the unified exchange mechanism based on exergy theory. The exchanged OMs (OM1, OM2, OM3, and OM4) are driven by exergy (Ex1, Ex2, Ex3, and Ex4) from various mechanisms, including aggregation/dissolution, adsorption/desorption, photochemistry, and biosynthesis/degradation. The exergy efficiencies (EFF) of the mechanisms are influenced by environmental factors, which are also driven by exergy. In the aquatic ecosystem, exergy sources are dominated by solar energy, tide energy, and earth radiant energy.

426

W. He et al. / Science of the Total Environment 551–552 (2016) 415–428

Fig. 6. Summary of analytical technologies in DOM-POM exchanges on the basis of size ranges (unit, meter, some parts are revised from Verdugo et al. (2004)). The width of band for each method denotes its applicable scale of size. Some analytical technologies (e.g. high performance liquid chromatography (HPLC), high performance size exclusion chromatography (HPSEC), high-performance anion-exchange chromatography pulsed amperometric detection, Fourier transform ion cyclotron resonance mass spectrometry, ultraviolet visible spectrometer (UV), fluorescence spectrometer (FS), spectrophotometric method, and ultrafiltration) are only used to determine DOM. Some (e.g. colorimetric method calibrated by gum xanthan, microscopic enumeration, X-ray diffraction & adsorption) are only suitable for POM detection. Some technologies, which have a large size detection range, can determine both DOM and POM. Among them, flow cytometry and dynamic (static) light scattering can provide a size distribution of organic matter. Atomic force microscopy gives images from molecular to particle. To determine the elemental composition, radiolabel 14C, total organic matter, and elemental analyzer are often used. For probing the chemical functional groups, pyrolysis gas chromatography mass spectrometry (py-GC/MS), Fourier transform infrared spectrophotometric analyzer (FTIR), and nuclear magnetic resonance (NMR) are often employed.

References Agatova, A.I., Dafner, E.V., Sapozhnikov, V.V., Torgunova, N.I., Ukolova, T.K., 1996. The trends of distribution of dissolved and particulate organic matter in the sea of Okhotsk. Okeanologiya 36, 856–864. Alldredge, A.L., Cowles, T.J., MacIntyre, S., Rines, J.E.B., Donaghay, P.L., Greenlaw, C.F., Holliday, D.V., Dekshenieks, M.M., Sullivan, J.M., Zaneveld, J.R.V., 2002. Occurrence and mechanisms of formation of a dramatic thin layer of marine snow in a shallow Pacific fjord. Mar. Ecol. Prog. Ser. 233, 1–12. Alvarez-Puebla, R.A., Garrido, J.J., 2005. Effect of pH on the aggregation of a gray humic acid in colloidal and solid states. Chemosphere 59, 659–667. Armstrong, R.A., Lee, C., Hedges, J.I., Honjo, S., Wakeham, S.G., 2002. A new, mechanistic model for organic carbon fluxes in the ocean based on the quantitative association of POC with ballast minerals. Deep-Sea Res. II Top. Stud. Oceanogr. 49, 219–236. Asmala, E., Bowers, D.G., Autio, R., Kaartokallio, H., Thomas, D.N., 2014. Qualitative changes of riverine dissolved organic matter at low salinities due to flocculation. J. Geophys. Res. Biogeosci. 119, 2014JG002722. Aufdenkampe, A.K., Hedges, J.I., Richey, J.E., Krusche, A.V., Llerena, C.A., 2001. Sorptive fractionation of dissolved organic nitrogen and amino acids onto fine sediments within the Amazon Basin. Limnol. Oceanogr. 46, 1921–1935. Azam, F., Malfatti, F., 2007. Microbial structuring of marine ecosystems. Nat. Rev. Microbiol. 5, 782–791. Baalousha, M., Motelica-Heino, M., Coustumer, P.L., 2006. Conformation and size of humic substances: effects of major cation concentration and type, pH, salinity, and residence time. Colloids Surf. A Physicochem. Eng. Asp. 272, 48–55. Bacastow, R., Maier-Reimer, E., 1991. Dissolved organic carbon in modeling oceanic new production. Glob. Biogeochem. Cycles 5, 71–85.

Baigorri, R., Fuentes, M., González-Gaitano, G., García-Mina, J.M., 2007. Analysis of molecular aggregation in humic substances in solution. Colloids Surf. A Physicochem. Eng. Asp. 302, 301–306. Benetoli, L.O.B., de Souza, C.M.D., da Silva, K.L., Souza, I.G.D., de Santana, H., Paesano, A., da Costa, A.C.S., Zaia, C., Zaia, D.A.M., 2007. Amino acid interaction with and adsorption on clays: FT-IR and Mossbauer spectroscopy and X-ray diffractometry investigations. Orig. Life Evol. Biosph. 37, 479–493. Bhaskar, P.V., Grossart, H.P., Bhosle, N.B., Simon, M., 2005. Production of macroaggregates from dissolved exopolymeric substances (EPS) of bacterial and diatom origin. FEMS Microbiol. Ecol. 53, 255–264. Biber, M.V., Gulacar, F.O., Buffle, J., 1996. Seasonal variations in principal groups of organic matter in a eutrophic lake using pyrolysis/GC/MS. Environ. Sci. Technol. 30, 3501–3507. Burd, A.B., Jackson, G.A., 2009. Particle aggregation. Ann. Rev. Mar. Sci. 1, 65–90. Bushaw, K.L., Zepp, R.G., Tarr, M.A., SchulzJander, D., Bourbonniere, R.A., Hodson, R.E., Miller, W.L., Bronk, D.A., Moran, M.A., 1996. Photochemical release of biologically available nitrogen from aquatic dissolved organic matter. Nature 381, 404–407. Cappiello, A., Trufelli, H., Famiglini, G., Pierini, E., Capellacci, S., Penna, A., Ricci, F., Ingarao, C., Penna, N., 2007. Study on the oligosaccharides composition of the water-soluble fraction of marine mucilage by electrospray tandem mass spectrometry. Water Res. 41, 2911–2920. Chen, H., Abdulla, H.A.N., Sanders, R.L., Myneni, S.C.B., Mopper, K., Hatcher, P.G., 2014. Production of black carbon-like and aliphatic molecules from terrestrial dissolved organic matter in the presence of sunlight and iron. Environ. Sci. Technol. Lett. 1, 399–404. Chin, W.C., Orellana, M.V., Verdugo, P., 1998. Spontaneous assembly of marine dissolved organic matter into polymer gels. Nature 391, 568–572.

W. He et al. / Science of the Total Environment 551–552 (2016) 415–428 Claret, F., Schäfer, T., Brevet, J., Reiller, P.E., 2008. Fractionation of Suwannee River fulvic acid and aldrich humic acid on α-Al2O3: spectroscopic evidence. Environ. Sci. Technol. 42, 8809–8815. Cottrell, B.A., Timko, S.A., Devera, L., Robinson, A.K., Gonsior, M., Vizenor, A.E., Simpson, A.J., Cooper, W.J., 2013. Photochemistry of excited-state species in natural waters: a role for particulate organic matter. Water Res. 47, 5189–5199. Dagg, M., Benner, R., Lohrenz, S., Lawrence, D., 2004. Transformation of dissolved and particulate materials on continental shelves influenced by large rivers: plume processes. Cont. Shelf Res. 24, 833–858. De La Rocha, C.L., Nowald, N., Passow, U., 2008. Interactions between diatom aggregates, minerals, particulate organic carbon, and dissolved organic matter: further implications for the ballast hypothesis. Glob. Biogeochem. Cycles 22. Debeljak, N., 2002. Applicability of genome size in exergy calculation. Ecol. Model. 152, 103–107. del Giorgio, P.A., Duarte, C.M., 2002. Respiration in the open ocean. Nature 420, 379–384. Determann, S., Reuter, R., Willkomm, R., 1996. Fluorescent matter in the eastern Atlantic Ocean. 2. Vertical profiles and relation to water masses. Deep-Sea Res. I Oceanogr. Res. Pap. 43, 345–360. Dewulf, J., Van Langenhove, H., Muys, B., Bruers, S., Bakshi, B.R., Grubb, G.F., Paulus, D.M., Sciubba, E., 2008. Exergy: its potential and limitations in environmental science and technology. Environ. Sci. Technol. 42, 2221–2232. Druffel, E.R.M., Williams, P.M., 1990. Identification of a deep marine source of particulate organic carbon using bomb 14C. Nature 347, 172–174. Druon, J.N., Mannino, A., Signorini, S., McClain, C., Friedrichs, M., Wilkin, J., Fennel, K., 2010. Modeling the dynamics and export of dissolved organic matter in the Northeastern US continental shelf. Estuar. Coast. Shelf Sci. 88, 488–507. Eadie, B.J., Morehead, N.R., Valklump, J., Landrum, P.F., 1992. Distribution of hydrophobic organic-compounds between dissolved and particulate organic-matter in Green Bay waters. J. Great Lakes Res. 18, 91–97. Eatherall, A., Naden, P.S., Cooper, D.M., 1998. Simulating carbon flux to the estuary: the first step. Sci. Total Environ. 210–211, 519–533. Engel, A., Thoms, S., Riebesell, U., Rochelle-Newall, E., Zondervan, I., 2004. Polysaccharide aggregation as a potential sink of marine dissolved organic carbon. Nature 428, 929–932. Engel, A., Piontek, J., Grossart, H.P., Riebesell, U., Schulz, K.G., Sperling, M., 2014. Impact of CO2 enrichment on organic matter dynamics during nutrient induced coastal phytoplankton blooms. J. Plankton Res. 36, 641–657. Eriksson, J., Frankki, S., Shchukarev, A., Skyllberg, U., 2004. Binding of 2,4,6-trinitrotoluene, aniline, and nitrobenzene to dissolved and particulate soil organic matter. Environ. Sci. Technol. 38, 3074–3080. Estapa, M.L., Mayer, L.M., 2010. Photooxidation of particulate organic matter, carbon/oxygen stoichiometry, and related photoreactions. Mar. Chem. 122, 138–147. Evans, C., Monteith, D., Cooper, D., 2005. Long-term increases in surface water dissolved organic carbon: observations, possible causes and environmental impacts. Environ. Pollut. 137, 55–71. Flynn, K.J., Clark, D.R., Xue, Y., 2008. Modeling the release of dissolved organic matter by phytoplankton. J. Phycol. 44, 1171–1187. Gao, H.Z., Zepp, R.G., 1998. Factors influencing photoreactions of dissolved organic matter in a coastal river of the southeastern United States. Environ. Sci. Technol. 32, 2940–2946. Gao, Q., Leck, C., Rauschenberg, C., Matrai, P.A., 2012. On the chemical dynamics of extracellular polysaccharides in the high Arctic surface microlayer. Ocean Sci. 8, 401–418. Giani, M., Savelli, F., Berto, D., Zangrando, V., Cosovic, B., Vojvodic, V., 2005. Temporal dynamics of dissolved and particulate organic carbon in the northern Adriatic Sea in relation to the mucilage events. Sci. Total Environ. 353, 126–138. Gogou, A., Repeta, D.J., 2010. Particulate-dissolved transformations as a sink for semilabile dissolved organic matter: chemical characterization of high molecular weight dissolved and surface-active organic matter in seawater and in diatom cultures. Mar. Chem. 121, 215–223. Goldthwait, S.A., Carlson, C.A., Henderson, G.K., Alldredge, A.L., 2005. Effects of physical fragmentation on remineralization of marine snow. Mar. Ecol. Prog. Ser. 305, 59–65. Grossart, H.P., Simon, M., 1998. Significance of limnetic organic aggregates (lake snow) for the sinking flux of particulate organic matter in a large lake. Aquat. Microb. Ecol. 15, 115–125. Gu, B., Schmitt, J., Chen, Z., Liang, L., McCarthy, J.F., 1994. Adsorption and desorption of natural organic matter on iron oxide: mechanisms and models. Environ. Sci. Technol. 28, 38–46. Hansell, D.A., Carlson, C.A., Repeta, D.J., Schlitzer, R., 2009. Dissolved organic matter in the ocean: a controversy stimulates new insights. Oceanography 22, 202–211. Hassett, J.P., 2006. Dissolved natural organic matter as a microreactor. Science 311, 1723–1724. Helms, J.R., Mao, J.D., Schmidt-Rohr, K., Abdulla, H., Mopper, K., 2013. Photochemical flocculation of terrestrial dissolved organic matter and iron. Geochim. Cosmochim. Acta 121, 398–413. Helms, J.R., Glinski, D.A., Mead, R.N., Southwell, M.W., Avery, G.B., Kieber, R.J., Skrabal, S.A., 2014. Photochemical dissolution of organic matter from resuspended sediments: impact of source and diagenetic state on photorelease. Org. Geochem. 73, 83–89. Hertkorn, N., Harir, M., Koch, B.P., Michalke, B., Schmitt-Kopplin, P., 2013. High-field NMR spectroscopy and FTICR mass spectrometry: powerful discovery tools for the molecular level characterization of marine dissolved organic matter. Biogeosciences 10, 1583–1624. Hopkinson, C.S., Vallino, J.J., 2005. Efficient export of carbon to the deep ocean through dissolved organic matter. Nature 433, 142–145. Hossler, K., Bauer, J.E., 2012. Estimation of riverine carbon and organic matter source contributions using time-based isotope mixing models. J. Geophys. Res. Biogeosci. 117. Hur, J., Jung, K.-Y., Schlautman, M.A., 2011. Altering the characteristics of a leaf litterderived humic substance by adsorptive fractionation versus simulated solar irradiation. Water Res. 45, 6217–6226.

427

Hwang, J., Druffel, E.R.M., 2003. Lipid-like material as the source of the uncharacterized organic carbon in the ocean? Science 299, 881–884. Hwang, J.S., Druffel, E.R.M., Bauer, J.E., 2006. Incorporation of aged dissolved organic carbon (DOC) by oceanic particulate organic carbon (POC): an experimental approach using natural carbon isotopes. Mar. Chem. 98, 315–322. Jackson, G.A., Burd, A.B., 1998. Aggregation in the marine environment. Environ. Sci. Technol. 32, 2805–2814. Jagadamma, S., Mayes, M.A., Phillips, J.R., 2012. Selective sorption of dissolved organic carbon compounds by temperate soils. PLoS One 7. Jiao, N., Herndl, G.J., Hansell, D.A., Benner, R., Kattner, G., Wilhelm, S.W., Kirchman, D.L., Weinbauer, M.G., Luo, T.W., Chen, F., Azam, F., 2010. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat. Rev. Microbiol. 8, 593–599. Johnson, B.D., Cooke, R.C., 1980. Organic particle and aggregate formation resulting from the dissolution of bubbles in seawater. Limnol. Oceanogr. 25, 653–661. Jørgensen, S.E., 1992. Exergy and ecology. Ecol. Model. 63, 185–214. Jørgensen, S.E., Svirezhev, Y.M., 2004. Towards a thermodynamic theory for ecological systems. Elsevier. Kaiser, K., Kaupenjohann, M., Zech, W., 2001. Sorption of dissolved organic carbon in soils: effects of soil sample storage, soil-to-solution ratio, and temperature. Geoderma 99, 317–328. Kang, S., Xing, B., 2008. Humic acid fractionation upon sequential adsorption onto goethite. Langmuir 24, 2525–2531. Karlsson, O.M., Richardson, J.S., Kiffney, P.A., 2005. Modelling organic matter dynamics in headwater streams of south-western British Columbia, Canada. Ecol. Model. 183, 463–476. Kepkay, P.E., 1994. Particle aggregation and the biological reactivity of colloids. Mar. Ecol. Prog. Ser. 109, 293–304. Kerner, M., Hohenberg, H., Ertl, S., Reckermann, M., Spitzy, A., 2003. Self-organization of dissolved organic matter to micelle-like microparticles in river water. Nature 422, 150–154. Kieber, R.J., Whitehead, R.F., Skrabal, S.A., 2006. Photochemical production of dissolved organic carbon from resuspended sediments. Limnol. Oceanogr. 51, 2187–2195. Kleber, M., Sollins, P., Sutton, R., 2007. A conceptual model of organo-mineral interactions in soils: self-assembly of organic molecular fragments into zonal structures on mineral surfaces. Biogeochemistry 85, 9–24. Koelmans, A.A., Prevo, L., 2003. Production of dissolved organic carbon in aquatic sediment suspensions. Water Res. 37, 2217–2222. Komada, T., Reimers, C.E., 2001. Resuspension-induced partitioning of organic carbon between solid and solution phases from a river-ocean transition. Mar. Chem. 76, 155–174. Kovac, N., Faganeli, J., Bajt, O., Sket, B., Orel, B., Penna, N., 2004. Chemical composition of macroaggregates in the northern Adriatic sea. Org. Geochem. 35, 1095–1104. Lara, R.J., Thomas, D.N., 1995. Formation of recalcitrant organic matter: humification dynamics of algal derived dissolved organic carbon and its hydrophobic fractions. Mar. Chem. 51, 193–199. Le Moigne, F.A.C., Gallinari, M., Laurenceau, E., De La Rocha, C.L., 2013. Enhanced rates of particulate organic matter remineralization by microzooplankton are diminished by added ballast minerals. Biogeosciences 10, 5755–5765. Lechtenfeld, O.J., Hertkorn, N., Shen, Y., Witt, M., Benner, R., 2015. Marine sequestration of carbon in bacterial metabolites. Nat. Commun. 6, 6711. Liang, L., Luo, L., Zhang, S.Z., 2011. Adsorption and desorption of humic and fulvic acids on SiO2 particles at nano- and micro-scales. Colloids Surf. A Physicochem. Eng. Asp. 384, 126–130. Loh, A.N., Canuel, E.A., Bauer, J.E., 2008. Potential source and diagenetic signatures of oceanic dissolved and particulate organic matter as distinguished by lipid biomarker distributions. Mar. Chem. 112, 189–202. Ma, Z.W., Gray, E., Thomas, E., Murphy, B., Zachos, J., Paytan, A., 2014. Carbon sequestration during the Palaeocene-Eocene Thermal Maximum by an efficient biological pump. Nat. Geosci. 7, 382–388. Mannino, A., Harvey, H.R., 1999. Lipid composition in particulate and dissolved organic matter in the Delaware Estuary: sources and diagenetic patterns. Geochim. Cosmochim. Acta 63, 2219–2235. Mao, J.D., Tremblay, L., Gagne, J.P., Kohl, S., Rice, J., Schmidt-Rohr, K., 2007. Humic acids from particulate organic matter in the Saguenay Fjord and the St. Lawrence Estuary investigated by advanced solid-state NMR. Geochim. Cosmochim. Acta 71, 5483–5499. Mari, X., Rochelle-Newall, E., Torreton, J.P., Pringault, O., Jouon, A., Migon, C., 2007. Water residence time: a regulatory factor of the DOM to POM transfer efficiency. Limnol. Oceanogr. 52, 808–819. Maurice, P.A., Lee, Y.J., Hersman, L.E., 2000. Dissolution of Al-substituted goethites by an aerobic Pseudomonas mendocina var. bacteria. Geochim. Cosmochim. Acta 64, 1363–1374. Mayer, L.M., Schick, L.L., Skorko, K., Boss, E., 2006. Photodissolution of particulate organic matter from sediments. Limnol. Oceanogr. 51, 1064–1071. Mayer, L.M., Schick, L.L., Hardy, K.R., Estapa, M.L., 2009. Photodissolution and other photochemical changes upon irradiation of algal detritus. Limnol. Oceanogr. 54, 1688–1698. Mayer, L.M., Thornton, K.H., Schick, L.L., 2011. Bioavailability of organic matter photodissolved from coastal sediments. Aquat. Microb. Ecol. 64, 275–284. Mayorga, E., Aufdenkampe, A.K., Masiello, C.A., Krusche, A.V., Hedges, J.I., Quay, P.D., Richey, J.E., Brown, T.A., 2005. Young organic matter as a source of carbon dioxide outgassing from Amazonian rivers. Nature 436, 538–541. McCarthy, M.D., Benner, R., Lee, C., Fogel, M.L., 2007. Amino acid nitrogen isotopic fractionation patterns as indicators of heterotrophy in plankton, particulate, and dissolved organic matter. Geochim. Cosmochim. Acta 71, 4727–4744.

428

W. He et al. / Science of the Total Environment 551–552 (2016) 415–428

McClain, M.E., Richey, J.E., Brandes, J.A., Pimentel, T.P., 1997. Dissolved organic matter and terrestrial-lotic linkages in the central Amazon basin of Brazil. Glob. Biogeochem. Cycles 11, 295–311. McKnight, D.M., Bencala, K.E., Zellweger, G.W., Aiken, G.R., Feder, G.L., Thorn, K.A., 1992. Sorption of dissolved organic carbon by hydrous aluminum and iron oxides occurring at the confluence of Deer Creek with the Snake River, Summit County, Colorado. Environ. Sci. Technol. 26, 1388–1396. Mecozzi, M., Pietrantonio, E., Di Noto, V., Papai, Z., 2005. The humin structure of mucilage aggregates in the Adriatic and Tyrrhenian seas: hypothesis about the reasonable causes of mucilage formation. Mar. Chem. 95, 255–269. Monteith, D.T., Stoddard, J.L., Evans, C.D., de Wit, H.A., Forsius, M., Høgåsen, T., Wilander, A., Skjelkvåle, B.L., Jeffries, D.S., Vuorenmaa, J., 2007. Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 450, 537–540. Moran, S.B., Buesseler, K.O., 1992. Short residence time of colloids in the upper ocean estimated from 238 U-234Th disequilibria. Nature 359, 221–223. Mukherjee, J., Ray, S., Ghosh, P.B., 2013. A system dynamic modeling of carbon cycle from mangrove litter to the adjacent Hooghly estuary, India. Ecol. Model. 252, 185–195. Myneni, S., Brown, J., Martinez, G., Meyer-Ilse, W., 1999. Imaging of humic substance macromolecular structures in water and soils. Science 286, 1335–1337. Osborne, T.Z., Inglett, P.W., Reddy, K.R., 2007. The use of senescent plant biomass to investigate relationships between potential particulate and dissolved organic matter in a wetland ecosystem. Aquat. Bot. 86, 53–61. Osburn, C.L., Handsel, L.T., Mikan, M.P., Paerl, H.W., Montgomery, M.T., 2012. Fluorescence tracking of dissolved and particulate organic matter quality in a river-dominated estuary. Environ. Sci. Technol. 46, 8628–8636. Oulehle, F., Hruška, J., 2009. Rising trends of dissolved organic matter in drinking-water reservoirs as a result of recovery from acidification in the Ore Mts., Czech Republic. Environ. Pollut. 157, 3433–3439. Passow, U., 2000. Formation of transparent exopolymer particles, TEP, from dissolved precursor material. Mar. Ecol. Prog. Ser. 192, 1–11. Passow, U., 2002. Transparent exopolymer particles (TEP) in aquatic environments. Prog. Oceanogr. 55, 287–333. Passow, U., 2012. The abiotic formation of TEP under different ocean acidification scenarios. Mar. Chem. 128, 72–80. Perez, M.A.P., Moreira-Turcq, P., Gallard, H., Allard, T., Benedetti, M.F., 2011. Dissolved organic matter dynamic in the Amazon basin: sorption by mineral surfaces. Chem. Geol. 286, 158–168. Piccolo, A., 2001. The supramolecular structure of humic substances. Soil Sci. 166, 810–832. Pisani, O., Yamashita, Y., Jaffé, R., 2011. Photo-dissolution of flocculent, detrital material in aquatic environments: contributions to the dissolved organic matter pool. Water Res. 45, 3836–3844. Porcal, P., Dillon, P.J., Molot, L.A., 2013. Photochemical production and decomposition of particulate organic carbon in a freshwater stream. Aquat. Sci. 75, 469–482. Post, W.M., Peng, T.H., Emanuel, W.R., King, A.W., Dale, V.H., Deangelis, D.L., 1990. The global carbon-cycle. Am. Sci. 78, 310–326. Pullin, M.J., Progess, C.A., Maurice, P.A., 2004. Effects of photoirradiation on the adsorption of dissolved organic matter to goethite. Geochim. Cosmochim. Acta 68, 3643–3656. Reid, P.M., Wilkinson, A.E., Tipping, E., Jones, M.N., 1991. Aggregation of humic substances in aqueous media as determined by light-scattering methods. J. Soil Sci. 42, 259–270. Remington, S.M., Strahm, B.D., Neu, V., Richey, J.E., da Cunha, H.B., 2007. The role of sorption in control of riverine dissolved organic carbon concentrations by riparian zone soils in the Amazon basin. Soil Sci. 172, 279–291. Roulet, N., Moore, T.R., 2006. Environmental chemistry: Browning the waters. Nature 444, 283–284. Sandvik, S.L.H., Bilski, P., Pakulski, J.D., Chignell, C.F., Coffin, R.B., 2000. Photogeneration of singlet oxygen and free radicals in dissolved organic matter isolated from the Mississippi and Atchafalaya River plumes. Mar. Chem. 69, 139–152. Sannigrahi, P., Ingall, E.D., Benner, R., 2006. Nature and dynamics of phosphoruscontaining components of marine dissolved and particulate organic matter. Geochim. Cosmochim. Acta 70, 5868–5882. Schartau, M., Engel, A., Schroter, J., Thoms, S., Volker, C., Wolf-Gladrow, D., 2007. Modelling carbon overconsumption and the formation of extracellular particulate organic carbon. Biogeosciences 4, 433–454. Schiebel, H.N., Wang, X., Chen, R.F., Peri, F., 2014. Photochemical release of dissolved organic matter from resuspended salt marsh sediments. Estuar. Coasts 1-14. Schindler, D.W., Curtis, P.J., 1997. The role of DOC in protecting freshwaters subjected to climatic warming and acidification from UV exposure. Biogeochemistry 36, 1–8. Schwesig, D., Kalbitz, K., Matzner, E., 2003. Effects of aluminium on the mineralization of dissolved organic carbon derived from forest floors. Eur. J. Soil Sci. 54, 311–322. Seitzinger, S.P., Harrison, J.A., Dumont, E., Beusen, A.H.W., Bouwman, A.F., 2005. Sources and delivery of carbon, nitrogen, and phosphorus to the coastal zone: an overview of Global Nutrient Export from Watersheds (NEWS) models and their application. Glob. Biogeochem. Cycles 19. Shank, G.C., Evans, A., Yamashita, Y., Jaffe, R., 2011. Solar radiation-enhanced dissolution of particulate organic matter from coastal marine sediments. Limnol. Oceanogr. 56, 577–588. Shiu, R.-F., Chin, W.-C., Lee, C.-L., 2014. Carbonaceous particles reduce marine microgel formation. Sci. Rep. 4, 5856. Sholkovitz, E.R., 1976. Flocculation of dissolved organic and inorganic matter during the mixing of river water and seawater. Geochim. Cosmochim. Acta 40 (7), 831–845.

Sholkovitz, E.R., Boyle, E.A., Price, N.B., 1978. The removal of dissolved humic acids and iron during estuarine mixing. Earth Planet. Sci. Lett. 40 (1), 130–136. Simon, M., Grossart, H.P., Schweitzer, B., Ploug, H., 2002. Microbial ecology of organic aggregates in aquatic ecosystems. Aquat. Microb. Ecol. 28, 175–211. Skoog, A., Benner, R., 1997. Aldoses in various size fractions of marine organic matter: implications for carbon cycling. Limnol. Oceanogr. 42, 1803–1813. Skoog, A., Hall, P.O.J., Hulth, S., Paxeus, N., vanderLoeff, M.R., Westerlund, S., 1996. Early diagenetic production and sediment-water exchange of fluorescent dissolved organic matter in the coastal environment. Geochim. Cosmochim. Acta 60, 3619–3629. Smith, D.C., Simon, M., Alldredge, A.L., Azam, F., 1992. Intense hydrolytic enzyme-activity on marine aggregates and implication for rapid particle dissolution. Nature 359, 139–142. Southwell, M.W., Mead, R.N., Luquire, C.M., Barbera, A., Avery, G.B., Kieber, R.J., Skrabal, S.A., 2011. Influence of organic matter source and diagenetic state on photochemical release of dissolved organic matter and nutrients from resuspendable estuarine sediments. Mar. Chem. 126, 114–119. Stordal, M.C., Santschi, P.H., Gill, G.A., 1996. Colloidal pumping: evidence for the coagulation process using natural colloids tagged with 203Hg. Environ. Sci. Technol. 30, 3335–3340. Susani, L., Pulselli, F.M., Jorgensen, S.E., Bastianoni, S., 2006. Comparison between technological and ecological exergy. Ecol. Model. 193, 447–456. Swan, C.M., Siegel, D.A., Nelson, N.B., Carlson, C.A., Nasir, E., 2009. Biogeochemical and hydrographic controls on chromophoric dissolved organic matter distribution in the Pacific Ocean. Deep-Sea Res. I Oceanogr. Res. Pap. 56, 2175–2192. Thornton, D.C.O., 2004. Formation of transparent exopolymeric particles (TEP) from macroalgal detritus. Mar. Ecol. Prog. Ser. 282, 1–12. Timko, S.A., Gonsior, M., Cooper, W.J., 2015. Influence of pH on fluorescent dissolved organic matter photo-degradation. Water Res. 85, 266–274. Tremblay, L., Gagne, J.P., 2009. Organic matter distribution and reactivity in the waters of a large estuarine system. Mar. Chem. 116, 1–12. van de Weerd, H., van Riemsdijk, W.H., Leijnse, A., 1999. Modeling the dynamic adsorption/desorption of a NOM mixture: effects of physical and chemical heterogeneity. Environ. Sci. Technol. 33, 1675–1681. VanHeemst, J.D.H., Peulve, S., DeLeeuw, J.W., 1996. Novel algal polyphenolic biomacromolecules as significant contributors to resistant fractions of marine dissolved and particulate organic matter. Org. Geochem. 24, 629–640. Varela, M.M., Bode, A., Gonzalez, N., Rodriguez, C., Varela, M., 2003. Fate of organic matter in the Ria de Ferrol (Galicia, NW Spain): uptake by pelagic bacteria vs. particle sedimentation. Acta Oecol.-Int. J. Ecol. 24, S77–S86. Verdugo, P., Santschi, P.H., 2010. Polymer dynamics of DOC networks and gel formation in seawater. Deep-Sea Res. II Top. Stud. Oceanogr. 57, 1486–1493. Verdugo, P., Alldredge, A.L., Azam, F., Kirchman, D.L., Passow, U., Santschi, P.H., 2004. The oceanic gel phase: a bridge in the DOM-POM continuum. Mar. Chem. 92, 67–85. Voelker, B.M., Morel, F.M., Sulzberger, B., 1997. Iron redox cycling in surface waters: effects of humic substances and light. Environ. Sci. Technol. 31, 1004–1011. von Wachenfeldt, E., Tranvik, L.J., 2008. Sedimentation in boreal lakes — the role of flocculation of allochthonous dissolved organic matter in the water column. Ecosystems 11, 803–814. Wang, G.S., Post, W.M., Mayes, M.A., 2013. Development of microbial-enzyme-mediated decomposition model parameters through steady-state and dynamic analyses. Ecol. Appl. 23, 255–272. Wells, M.L., 1998. Marine colloids - A neglected dimension. Nature 391, 530–531. Wershaw, R.L., 1999. Molecular aggregation of humic substances. Soil Sci. 164, 803–813. Wershaw, R.L., Leenheer, J.A., Sperline, R.P., Song, Y.A., Noll, L.A., Melvin, R.L., Rigatti, G.P., 1995. Mechanism of formation of humus coatings on mineral surfaces. 1. Evidence for multidentate binding of organic-acids from compost leachate on alumina. Colloids Surf. A Physicochem. Eng. Asp. 96, 93–104. Wetz, M.S., Wheeler, P.A., 2007. Release of dissolved organic matter by coastal diatoms. Limnol. Oceanogr. 52, 798–807. Wetz, M.S., Hales, B., Wheeler, P.A., 2008. Degradation of phytoplankton-derived organic matter: implications for carbon and nitrogen biogeochemistry in coastal ecosystems. Estuar. Coast. Shelf Sci. 77, 422–432. Wetzel, R.G., 1995. Death, detritus, and energy-flow in aquatic ecosystems. Freshw. Biol. 33, 83–89. Wotton, R.S., 2004. The ubiquity and many roles of exopolymers (EPS) in aquatic systems. Sci. Mar. 68, 13–21. Yamanaka, Y., Tajika, E., 1997. Role of dissolved organic matter in the marine biogeochemical cycle: studies using an ocean biogeochemical general circulation-model. Glob. Biogeochem. Cycles 11, 599–612. Yang, X.F., Li, Z.Q., Meng, F.G., Wang, Z.G., Sun, L., 2014. Photochemical alteration of biogenic particles in wastewater effluents. Chin. Sci. Bull. 59, 3659–3668. Yoshimura, C., Fujii, M., Omura, T., Tockner, K., 2010. Instream release of dissolved organic matter from coarse and fine particulate organic matter of different origins. Biogeochemistry 100, 151–165. Zielińska, K., Town, R.M., Yasadi, K., van Leeuwen, H.P., 2014. Partitioning of humic acids between aqueous solution and hydrogel: concentration profiling of humic acids in hydrogel phases. Langmuir 30, 2084–2092. Zimmermann-Timm, H., 2002. Characteristics, dynamics and importance of aggregates in rivers — an invited review. Int. Rev. Hydrobiol. 87, 197–240.