The effect of soil horizon and mineral type on the distribution of siderophores in soil

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ScienceDirect Geochimica et Cosmochimica Acta 131 (2014) 184–195 www.elsevier.com/locate/gca

The effect of soil horizon and mineral type on the distribution of siderophores in soil Engy Ahmed ⇑, Sara J.M. Holmstro¨m 1 Department of Geological Sciences, Stockholm University, SE-10691 Stockholm, Sweden Received 29 March 2013; accepted in revised form 27 January 2014; available online 1 February 2014

Abstract Iron is a key component of the chemical architecture of the biosphere. Due to the low bioavailability of iron in the environment, microorganisms have developed specific uptake strategies like production of siderophores. Siderophores are operationally defined as low-molecular-mass biogenic Fe(III)-binding compounds, that can increase the bioavailability of iron by promoting the dissolution of iron-bearing minerals. In the present study, we investigated the composition of dissolved and adsorbed siderophores of the hydroxamate family in the soil horizons of podzol and the effect of specific mineral types on siderophores. Three polished mineral specimens of 3 cm  4 cm  3 mm (apatite, biotite and oligioclase) were inserted in the soil horizons (O (organic), E (eluvial) and B (upper illuvial)). After two years, soil samples were collected from both the bulk soil of the whole profile and from the soil attached to the mineral surfaces. The concentration of ten different fungal tri-hydroxamates within ferrichromes, fusigen and coprogens families, and five bacterial hydroxamates within the ferrioxamine family were detected. All hydroxamate types were determined in both soil water (dissolved) and soil methanol (adsorbed) extracts along the whole soil profile by high-performance liquid chromatography coupled to electrospray ionization mass spectrometry (HPLC–ESI-MS); hence, the study is the most extensive of its kind. We found that coprogens and fusigen were present in much higher concentrations in bulk soil than were ferrioxamines and ferrichromes. On the other hand, the presence of the polished mineral completely altered the distribution of siderophores. In addition, each mineral had a unique interaction with the dissolved and adsorbed hydroxamates in the different soil horizons. Thus siderophore composition in the soil environment is controlled by the chemical, physical and biological characteristics of each soil horizon and also by the available mineral types. Ó 2014 Elsevier Ltd. All rights reserved.

1. INTRODUCTION In the soil environment, the microbial communities that colonize mineral surfaces differ from those of the surrounding soil particles (Certini et al., 2004). Microbial attachment to mineral surfaces leads to the formation of a microenvironment that protects the microorganisms against environmental stress (Beveridge et al., 1997; Liermann et al., 2000a; ⇑ Corresponding author. Tel.: +46 (0)8 674 7725; fax: +46 (0)8

674 7897. E-mail addresses: [email protected] (E. Ahmed), sara. [email protected] (S.J.M. Holmstro¨m). 1 Tel.: +46 (0)8 674 4751; fax: +46 (0)8 674 7897. http://dx.doi.org/10.1016/j.gca.2014.01.031 0016-7037/Ó 2014 Elsevier Ltd. All rights reserved.

Ojeda et al., 2006). In the microenvironments, mineral nutrients can be chelated directly from the soil minerals by certain microorganisms or shared among the surrounding microorganisms (Brown et al., 1994; Rogers et al., 1998; Roberts Rogers et al., 2001; Bennett et al., 2001; Roberts Rogers and Bennett, 2004). Most soil microorganisms can promote mineral weathering by production of siderophores which are defined as low-molecular-mass Fe(III)-binding compounds. Siderophores provide an efficient Fe-acquisition system due to their high affinity for Fe(III) complexation resulting in mineral dissolution (Kraemer, 2004). In soils that are enriched with iron oxide and clay silicate mineral phases, siderophores play a significant role in iron dissolution, making it available for microorganisms and

E. Ahmed, S.J.M. Holmstro¨m / Geochimica et Cosmochimica Acta 131 (2014) 184–195

plants (Hersman et al., 1995). There are several mechanisms for siderophore promoted iron dissolution (e.g., Holme´n and Casey, 1996, 1998). The general mechanism is that the Fe-siderophore complex is formed at the mineral surface and is then transferred into the surrounding soil solution, thereby becoming available for uptake by the cell membrane of microorganisms or plants (Kalinowski et al., 2000a; Liermann et al., 2000b; Kraemer, 2004). Siderophores are either recycled or destroyed upon iron reduction, whereas the reduced iron Fe(II) that is not used by the cell can act as an electron donor in electron transport chains (Kalinowski et al., 2000b). The impact of siderophores on soil mineral weathering can be more effective compared to that of organic acids since siderophores form more stable complexes with Fe(III). Siderophores form 1:1 complexes with Fe(III), with binding constants ranging between K = 1030 and K = 1052 (Jalal and van der Helm, 1991; Matzanke, 1991), while the binding constants of oxalic and citric acids with Fe(III) are K = 107.6 and 1012.3, respectively (Perrin, 1979). The ligand protonation constant (pKa) values of siderophores were estimated between 7.3 and 13 dependent on the siderophore type (Raymond et al., 1984), whereas the pKa values of organic acids were ranged between 2.5 and 6.5 according to the acid type (Banaszak et al., 1999). Microorganisms produce a wide range of siderophore types. Most of the bacterial siderophores are catecholates, and some of them are trihydroxamates and carboxylates, whereas most of fungal siderophores are hydroxamates (Schalk et al., 2011). The trihydroxamate ferrioxamine is produced by many soil bacteria, such as Erwinia, Nocardia, Streptomyces, Arthrobacter, Chromobacterium and Pseudomonas species (Meyer and Abdallah, 1980; Muller and Raymond, 1984; Berner et al., 1988; Gunter et al., 1993; Wei et al., 2007). In contrast, most hydroxamate siderophores produced by soil fungal species (i.e. Suillus granulatus, Fusarium spp and Aspergillus spp.) are of the ferrichrome family. Ferrichromes are divided into five groups depending on the side chain of the hydroxamate functional group: acetyl (ferrichrome, ferrichrome C, ferricrocin and ferrichrysin), malonyl (malonichrome), trans-bmethylglutaconyl (ferrichrome A), trans-anhydromevalonyl (ferrirubin) and cis-anhydromevalonyl (ferrirhodin) (Winkelmann and Huschka 1987; Renshaw et al., 2002). Due to the importance of microbial siderophores in weathering and soil formation, the role of siderophores in the dissolution of iron minerals has been investigated intensively (Inoue et al., 1993; Watteau and Berthelin, 1994; Hersman et al., 1995; Hiradate and Inoue, 1998; Holme´n and Casey, 1996, 1998; Kraemer et al., 1999; Liermann et al., 2000a; Kalinowski et al., 2000a; Stone, 1997; Reichard et al. 2005; Buss et al., 2007; Shirvani and Nourbakhsh, 2010). Hydroxamate siderophores produced by the ectomycorrhizal fungus Suillus granulatus are very efficient in the dissolution of goethite. High quantities (109 mol m2 h1) of iron have been demonstrated to be mobilized in the presence of Suillus sp. because of the continuous production of siderophores (Watteau and Berthelin, 1994). Mineral dissolution is enhanced not only by siderophore-producing fungi but also by bacteria such as Bacillus sp., which have been documented to produce siderophores that promoted the

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dissolution of the surface of hornblende (Buss et al., 2007). The dissolution of Fe from the hornblende has been also observed in the presence of siderophore-producing actinomycetes such as Streptomyces and Arthrobacter (Kalinowski et al., 2000b). Therefore, the interactions between siderophores and iron minerals are directly related to the iron acquisition efficiency of the living cells in the soil environment (Shirvani and Nourbakhsh, 2010). For example, fungal siderophores (i.e. ferrichrome and ferricrocin) have been found to play a significant role in changing the surface structure of biotite and increasing its dissolution in podzolic forest soil (Sokolova et al., 2010). Few studies have discussed the concentrations of siderophore in podzolic soil solution (Holmstro¨m et al., 2004; Esse´n et al., 2006; Ali et al., 2011). Many gaps still remain in understanding the relationship between siderophore content and mineral weathering in the field. Due to the wide variation of the chemical properties (e.g. pH and mineral nutrients) and microbial composition of each horizon in the podzol soil, the present study aimed to answer several questions: (1) How do the podzol soil horizon characteristics affect the concentration and distribution of hydroxamates? (2) Could the presence of different mineral types change the concentration and distribution of hydroxamates? (3) In which phase, dissolved or adsorbed, can siderophores be found in soil? 2. MATERIALS AND METHODS 2.1. Sampling site Soils were sampled in September 2011 from central Sweden in the vicinity of the village Bispga˚rden (63°070 N, 16°700 E). The site is located on a slope (angle 2°) at an altitude of 258 m above sea level and is forested with 80-yr-old Norway spruce (Picea abies) and Scots pine (Pinus sylvestris). The annual average precipitation is 700 mm, and is not acidic. The annual average temperature is +2 °C. The bedrock in the area is granite and gneiss. The soil is a typical haplic podzol (FAO, 1990). The soil horizons in the studied soil profile have the following depths: 12 cm for O (organic horizon), 10 cm for E (elluvial horizon), 9 cm for B (upper illuvial horizon) and finally C (parent material). Three polished minerals: biotite (purchased from Words, Canada), apatite and oligioclase (purchased from Krantz, Germany) with dimensions of 3 cm  4 cm  3 mm were used. The minerals were polished with 6, 3 and 1 lm diamond paste to get a fresh un-weathered surface. The three minerals were buried into the O-, E- and B-horizons at depths of 7, 14 and 28 cm, respectively from the top of the soil at June 2009 by Olofsson et al. (in preparation). The soil samples for this study were taken from the bulk soil of the whole profile and mineral surfaces and kept cold (+4 °C) until further analysis. The soil samples of each horizon were characterized chemically (Table 1). 2.2. Extraction of dissolved and adsorbed siderophores from soil For extraction of dissolved siderophores, 1 g of air dried soil sample was added to 10 ml of Milli Q-water and shaken

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Table 1 The chemical characterization of the whole podzol soil profile; (O) organic horizon, (E) elluvial horizon, (B) illuvial horizon and C parent material. The average content of exchangeable cations (lmol/g) was determined. Carbon (C%), nitrogen (N%) and moisture (%) content were also estimated. Podzol Horizons

Ca , %

Na, %

Caa, lmol/ g

Ka, lmol/ g

Mga, lmol/ g

Naa, lmol/ g

Feb, lmol/ g

pHb

Moistureb content, %

O E B C

47 0.93 1.9 0.3

1.2 0.03 0.06 0.01

1.7 1.7 1.5 1.3

0.5 0.5 0.3 0.2

0.5 0.5 0.3 0.2

0.2 0.2 0.2 0.2

0.3 0.3 0.2 0.09

4.4 4.6 5.1 5.4

89 86 78 26

a b

Vestin et al., 2008. The present study.

vigorously for 2 h. The soil solutions were then filtrated through 0.45 lm filters (Filtropur S, Sarstedt, Germany). For extraction of adsorbed siderophores, 1 g of air dried soil sample was added to 10 ml of methanol and shaken for 2 h. The soil solutions were then filtrated through 0.45 lm filters. The methanol filtrates were evaporated using rotary evaporation (Laborota 4001-efficient, Heidolph instruments), then the remaining residues were dissolved in Milli-Q water. The water extracts were pre-concentrated by freeze-drying (Scanvac cool Safe, 100-9 Pro). When all water in the sample had been evaporated a yellow–white, solid dust remained that was dissolved in 1 ml of Milli Q-water. To remove the high molecular mass compounds (>3000 Da), centrifugal ultrafiltration (3000 Da cutoff) filters (Nanosep 3 K Omega, Pall, Mexico) were used. Thereafter extracts were stored at 20 °C until further analysis. The pre-concentration and purification method was developed by Holmstro¨m et al. (2004). 2.3. Quantification and structure identification of the siderophores using HPLC–ESI-MS The extracted siderophores were analyzed using a method modified from Duckworth et al. (2009). Components of the HPLC system (Ultimate 3000 RS, Thermo Scientific, USA) included two pumps with flow rates of 0.030 ml/ min for the low pressure gradient pump and of 0.15 ml/ min for the high pressure gradient pump. The column compartment (Dionex Ultimate 3000, Thermo Scientific, USA) was set at 10 °C. The injection volume of standards and samples was 100 ll. The pre-column was a Syncronis C18 (50 mm  2.1 mm, particle size 1.7 lm, Thermo Scientific, USA) and the separation column was a Hypersil GOLD (100 mm  2.1 mm, particle size 1.9 lm, Thermo Scientific, USA). The pre-column was eluted to waste with mobile phase A (11 mM ammonium formate buffer, pH 4.0 and 1% v/v methanol) in order to concentrate and purify the hydroxamate siderophores. After 20 min, the pre-column was followed by back flushing towards the analytical column with a gradient of mobile phase B (11 mM ammonium formate buffer, pH 4.0 and 15% v/v acetonitrile) and mobile phase C (11 mM ammonium formate buffer, pH 4.0 and 5% v/v acetonitrile). The total analysis time was 60 min. The ferric complexes of the tri-hydroxamate siderophores, including ferrichromes, ferrioxamines, coprogens and fusigen (Fig. 1), were detected by selected ion monitoring

(SIM) of the proton adducts [M+H]+: i.e. m/z 797.3 for Tetraglycyl Ferrichrome, 771.3 for Ferricrocin, 741.2 for Ferrichrome, 801.2 for Ferrichrysin, 1011.3 for Ferrirubin, 1011.2 for Ferrirhodin, 1052.2 for Ferrichrome A, 614.2 for Ferrioxamine B, 672.2 for Ferrioxamine G, 656.3 for Ferrioxamine D, 654.3 for Ferrioxamine E, 682.5 for Neocoprogen II, 793.2 for Fusigen (lin.), 752.3 for Neocoprogen I, and 821.2 for Coprogen on a triple quadropole mass spectrometer (TSQ Quantum Access Max, Thermo Scientific, USA). 2.4. Data analysis and statistics The data were normalized and statistically evaluated with the principal component analysis (PCA) by using XLSTAT (http://www.xlstat.com/en/). The PCA was investigated for different parameters i.e., dissolved and adsorbed siderophore content in bulk soil with different soil horizons or/and mineral surfaces. The sum of Tetraglycyl ferrichrome, Ferricrocin, Ferrichrome, Ferrichrysin, ferrirubin, Ferrirhodin and Ferrichrome A was calculated and denoted as the total concentration of ferrichrome siderophores. The sum of Ferrioxamine B, Ferrioxamine G, Ferrioxamine D and Ferrioxamine E corresponds to the total concentration of ferrioxamines. The sum of Neocoprogen II, Neocoprogen I and Coprogen was denoted as the total concentration of coprogens. Fusigen (linear) represents the fusigen. We also calculated the sum of all the fifteen different types of siderophore that were analyzed in the present study as the total concentration of hydroxamate siderophores. 3. RESULTS 3.1. Siderophore concentration and distribution in podzol soil Dissolved and adsorbed ferrioxamines, ferrichromes, fusigen and coprogens concentration of podzolic soil samples were measured by HPLC–ESI-MS. The average concentration of total dissolved ferrioxamines was between 2 and 7 pmol/g dry soil; 1–4 pmol/g dry soil for ferrichromes; 0–39 pmol/g dry soil for fusigen and 0–14 pmol/g dry soil for coprogens (Fig. 2a). Maximum concentrations of dissolved ferrioxamines, fusigen and coprogens were found in the E-horizon, whereas the maximum concentration of the ferrichromes was found in the B-horizon. The average

E. Ahmed, S.J.M. Holmstro¨m / Geochimica et Cosmochimica Acta 131 (2014) 184–195

Ferrioxamine B (KFe(III)=30.5)

Ferrioxamine G (KFe(III)=30.8)

Ferrioxamine E(KFe(III)=32.4)

187

Fusigen (KFe(III)=31.2)

2

1

Ferrioxamine D (KFe(III)=30.6)

Ferrichrome (KFe(III)=29.1)

Coprogens (KFe(III)=30.2)

Ferrirhodin (KFe(III)=30.0)

Ferrichrome A (KFe(III)=32.0)

Tetraglycylferrichrome (KFe(III)=30.2)

2 3

1

Ferrichrysin (KFe(III)=30.0)

Ferricrocin (KFe(III)=30.4)

Ferrirubin (KFe(III)=30.1)

Fig. 1. Chemical structure of the analyzed hydroxamate siderophores with the stability constants of each type. Bacterial hydroxamates include Ferrioxamine (B, E, D and G). Fungal hydroxamates are Tetraglycyl Ferrichrome, Ferricrocin, Ferrichrome, Ferrichrysin, Ferrirubin, Ferrirhodin, Ferrichrome A, Fusigen (linear) and Coprogens. The chemical stuctures of the individual types of Coprogens are: Coprogen: R1 = H, R2 = COCH3, R3 = R4 = H; Neocoprogen I: R1 = H, R2 = COCH3, R3 = CH3, R4 = H and Neocoprogen: II R1 = H, R2 = COCH3, R3 = R4 = CH3. For Ferrirhodin R1 = R2 = CH2OH and for Ferrirubin R1 = R2 = CH2OH, R3 = H. All the chemical structures were drawn using ChemDraw Standard 13.0 software.

concentration of total dissolved hydroxamates was between 10 and 63 pmol/g dry soil and the maximum concentration was found in the E-horizon (Fig. 2b). We performed PCA analysis of the samples based on their composition of dissolved hydroxamate siderophore types. The first principal component was correlated with soil horizon (PC1, eigenvalue 14%) and the second principal component was correlated with hydroxamate types (PC2, eigenvalue 59%). As shown in the PCA biplot, the soil horizons have a strong influence on the dissolved hydroxamates distribution (Fig. 2c). All the individual ferrioxamines were correlated to the E-horizon. However, most of ferrichromes and coprogens were correlated to the O-horizon except for tetraglycl ferrichrome to the C-horizon and ferrirhodin to the E-horizon. Fusigen was correlated to the C-horizon.

Adsorbed hydoxamates were present in lower concentration than the dissolved hydroxamates. The average concentration of total adsorbed ferrioxamines was between 0 and 2 pmol/g dry soil; ferrichromes 0.3–2 pmol/g dry soil; fusigen 0–32 pmol/g dry soil and coprogens 0–13 pmol/g dry soil (Fig. 3a). Adsorbed hydroxamates were present in all investigated soil horizons, except for ferrioxamines and fusigen which were completely absent in the C-horizon. The maximum concentration of adsorbed ferrioxamines, ferrichromes, fusigen and coprogens were found in the E-horizon. The average concentration of total adsorbed hydroxamates for each soil horizon was between 8 and 51 pmol/g dry soil, with the maximum concentration in the E-horizon (Fig. 3b) being consistent with measurements for the individual groups of hydroxamates. The PCA

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A

A

Concentraon (pmol/g dry soil) 0

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C

C

B 10

O

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30

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B

60

70

20

30

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Total hydroxamates (pmol/g dry soil) 20 40 60

0

80

70

80

O

Soil horizons

O Soil horizons

B

C

Total hydroxamates (pmol/g dry soil) 0

E

E

Soil horizons

B

B

O

B

E

E

10

Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens

C

O

Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens

O

Soil horizons

10

Concentraon (pmol/g dry soil) 0

E

B

E

B

C C

C4

Biplot (axes F1 and F2: 73.03 %)

C4

Biplot (axes F1 and F2: 81.67 %)

E O 3

C

C F2 (14.05 %)

Neocoprogen II Ferrirhodin E Ferrioxamine E Ferrioxamine G E D Ferrioxamine Ferrioxamine B Coprogen

Fusigen (lin.) Tetraglycyl ferrichrome

CC

0

E

B B B B

O Neooprogen I

2

O

E

Ferrichrome A O O Ferrirubin O Ferrrichrysin Neooprogen I Ferrichrome O Ferricrocin

OB

-2

E

F2 (11.34 %)

2

O

1

Ferrichrome Fusigen (lin.) O Ferrioxamine G E Ferrichrome A Coprogen Ferrrichrysin Ferricrocin Neocoprogen II E Ferrioxamine D Ferrioxamine E Ferrioxamine B E

O 0

C CC B BB B B C B -1

Tetraglycyl ferrichrome Ferrirubin Ferrirhodin

E

O

E

E

B -2 -4 -6

-4

-2

0

2

4

6

F1 (58.99 %)

Fig. 2. The dissolved hydroxamates concentration (pmol/g dry soil) per each soil horizon as (A) individual hydroxamate groups (ferrioxamines, ferriochromes, fusigen and coprogens), (B) total hydroxamate concentration and (C) the principal component analysis (PCA) ordination of dissolved hydroxamates and soil horizons with total contribution of observation 73%. O, E, B and C referred to the soil horizons.

ordination was based on the composition of adsorbed hydroxamate types. The first principal component correlated with soil horizon (PC1, eigenvalue 11%) and the second principal component correlated with hydroxamate types (PC2, eigenvalue 70%). Based on the PCA, higher correlation was found between the distributions of adsorbed hydroxamates within each soil horizon (Fig. 3c) than of the dissolved hydroxamates (Fig. 2c). Therefore, most of the ferrichromes and all the ferrioxamines correlated to the E-horizon. However, ferrichrome, fusigen and

-3 -3

-2

-1

0

1

2

3

4

5

6

F1 (70.32 %)

Fig. 3. The adsorbed hydroxamates concentration (pmol/g dry soil) per each soil horizon as (A) individual hydroxamate groups (ferrioxamines, ferriochromes, fusigen and coprogens), (B) total hydroxamate concentration and (C) the principal component analysis (PCA) ordination of of adsorbed hydroxamates and soil horizons with total contribution of observation 82%. O, E, B and C referred to the soil horizons.

coprogens correlated to the O-horizon except tetraglycl ferrichrome and ferrihodin that correlated to the B- and C-horizons, respectively. 3.2. Siderophore concentration and distribution on the buried polished mineral surfaces Dissolved and adsorbed hydroxamates were also extracted and quantified from the soil attached to the

E. Ahmed, S.J.M. Holmstro¨m / Geochimica et Cosmochimica Acta 131 (2014) 184–195

A

Total hydroxamates (pmol/g dry soil) 0

20

40

60

80

100 120 140 160 180 200

Apate Biote

Minerals per each horizon

O

Oligioclase Apate Biote

E

Oligioclase Apate Biote

B

Oligioclase

B

Concentraon (pmol/g dry soil) 0

40

60

80

100

Apate Biote Oligioclase Apate Oligioclase Apate Biote Oligioclase

Biplot (axes F1 and F2: 68.84 %)

6

O_Bio

4

2

20

Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens

Biote

Minerals per each horizon

C

F2 (17.20 %)

surfaces of the three different mineral types that had been buried for two years in the three top horizons of podzol soil. The distribution of hydroxamates attached to mineral surfaces was completely different compared to the distribution within the bulk soil; in addition, to the concentrations were much higher. We found that the average concentration of total dissolved hydroxamates was between 20 and 83 pmol/g dry soil for apatite and the maximum concentration was found in the B-horizon (Fig. 4a). The total dissolved hydroxamates concentration was much higher on biotite (42–171 pmol/g dry soil) than the other minerals and the maximum concentration was found in the O-horizon. The minimum concentration of total dissolved hydroxamates was found on oligioclase (18–36 pmol/g dry soil). As shown in Fig. 4b, ferrichromes and fusigen have the highest concentration in the presence of biotite in O-horizon (66 pmol/g dry soil and 60 pmol/g dry soil, respectively). Coprogens have the highest concentration in the presence of apatite in B-horizon (67 pmol/g dry soil). The PCA ordination for these samples was based on all dissolved hydroxamate siderophore types along the first principal component (PC1, eigenvalue 53%), and the different mineral types within each podzol soil horizon along the second principal component (PC2, eigenvalue 17%) (Fig. 4c). The mineral type influenced the distribution of dissolved hydroxamates in a different way than what soil horizon did. Ferrioxamine E and B were correlated to the presence of the biotite and apatite in the E-horizon. Ferrioxamine G and D, ferrichrome and ferrirhodin were correlated to apatite in Oand B-horizons. Tetraglycyl ferrichrome was correlated to oligioclase in all soil horizons and the remaining hydroxamates were correlated to the presence of biotite in the O- and B-horizons. We also found that the dissolved hydoxamates concentration was higher than the concentration of adsorbed hydoxamates in the soil attached to the mineral surfaces. The average concentration of total adsorbed hydroxamates was between 35 and 64 pmol/g dry soil for apatite; 6– 55 pmol/g dry soil for biotite and 0.009–21 pmol/g dry soil for oligioclase (Fig. 5a). The maximum concentration was found in E-horizon for all of the minerals. Fusigen and coprogens were found in higher concentrations than ferrichromes and ferrioxamines for all mineral surfaces except the high concentration of ferrichromes with biotite in the O-horizon (Fig. 5b). Fusigen and coprogens were absent only on oligioclase in the O-horizon. The PCA ordination was based on all adsorbed hydroxamate siderophore types along the first principal component (PC1, eigenvalue 64%), and different mineral types within each podzol soil horizons along the second principal component (PC2, eigenvalue 17%). Based on PCA, it was obvious that apatite, biotite and oligioclase that were in the E-horizon influenced the distribution of all the adsorbed hydroxamates. Therefore, tetraglycyl ferrichrome, ferrioxamine G and B, ferrichrome A, coprogen, neocoprogen II and fusigen were correlated to the presence of apatite in the E-horizon, while the rest of the hydroxamates correlated to biotite and oligioclase in the same horizon, in addition to the apatite in O-horizon (Fig. 5c).

189

O_Bio

Neocoprogen II Fusigen (lin.)

Neooprogen I E_Bio E_Bio Ferrioxamine E Ferrirhodin Ferrrichrysin Ferrioxamine B

B_Bio B_Bio Ferrichrome A

0

Ferrioxamine G Ferricrocin B_Ap Ferrichrome Ferrioxamine D Coprogen Ferrirubin B_Ap O_Ap

E_Olig O_OligE_Olig O_Olig

-2

E_Ap E_Ap

B_Olig Tetraglycyl ferrichrome B_Olig

O_Ap

-4 -4

-2

0

2

4

6

8

10

F1 (51.64 %)

Fig. 4. The dissolved hydroxamate concentration (pmol/g dry soil) of soil attached on mineral surfaces per each soil horizon as (A) total hydroxamate concentration, (B) individual hydroxamate groups (ferrioxamines, ferriochromes, fusigen and coprogens) and (C) the principal component analysis (PCA) ordination of dissolved hydroxamates and mineral type per each soil horizon with total contribution of observation 69%. O, E and B referred to the soil horizons. Ap, Bio and Olig referred to apatite, biotite and oligioclase.

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A

4. DISCUSSION

Total hydroxamates (pmol/g dry soil) 0

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4.1. Siderophores in the soil environment

Minerals per each horizon

Apate Biote

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Biote Oligioclase

B

Concentraon (pmol/g dry soil)

0 Apate Biote Apate Biote Oligioclase

Apate

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Biote

Minerals per each horizon

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C

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30

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Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens Ferrioxamines Ferrichromes Fusigen Coprogens

Oligioclase

O

10

Biplot (axes F1 and F2: 81.35 %)

5 E_Ap

4

F2 (17.32 %)

3

E_Ap Tetraglycyl ferrichrome Ferrioxamine G Fusigen (lin.)

2 1

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0 B_Olig

-1

Neocoprogen II Coprogen Ferrichrome A Ferrioxamine B

B_Bio O_Bio

Ferrirubin Ferrioxamine E Ferrirhodin E_Olig Ferricrocin Ferrioxamine D O_Ap E_Olig O_Ap Ferrrichrysin Neooprogen I

O_Bio B_Ap B_Bio B_Ap

-2

E_Bio

Ferrichrome E_Bio

-3 -4

-3

-2

-1

0

1

2

3

4

5

6

F1 (64.02 %)

Fig. 5. The adsorbed hydroxamate concentration (pmol/g dry soil) of soil attached on mineral surfaces per each soil horizon as (A) total hydroxamate concentration, (B) individual hydroxamate groups (ferrioxamines, ferriochromes, fusigen and coprogens) and (C) the principal component analysis (PCA) ordination of adsorbed hydroxamates and mineral type per each soil horizon with total contribution of observation 81%. O, E and B referred to the soil horizons. Ap, Bio and Olig referred to apatite, biotite and oligioclase.

The presence of siderophores in soil has been earlier estimated by using microbial assays that revealed only the total concentration of hydroxamates, as well as ferrichrome-type siderophores. Powell et al. (1982, 1983) were the first who use these assays to quantitate the siderophores from dried sandy clay loam soil–water extracts. Powell et al. (1982) found that the total hydroxamates concentration was relatively high (up to 279 nM), reported as DFOB equivalents, while Powell et al. (1983) estimated 34 nM of total hydroxamate siderophores by using the M. flavescens assay and 78 nM of ferrichrome type by the E. coli assay. These studies which used microbial assays estimated much higher concentrations of the total dissolved hydroxamates than our present findings (10–63 nM) using HPLC–ESI-MS. However, we detected higher concentrations than those in other studies that measured hydroxamates in the range between 0.09 and 0.75 nM (Akers 1983) and between 0.2 and 0.5 nM in soils (Buyer et al. 1993). Dissolved individual hydroxamate siderophores concentration in Swedish podzolic forest soils has been measured using HPLC–MS previously in few studies (Holmstro¨m et al., 2004; Esse´n et al., 2006; Ali et al., 2011), in which much lower concentrations were estimated compared to those in studies using the microbial assays. Hydroxamates identified as ferrichrome and ferricrocin have been detected to be between 0.9 and 1.4 nM in soil solutions in the O-horizon of podzol soil at Potta¨ng, Sundsvall (Holmstro¨m et al., 2004), similar to what was found in our study. We found 0.06–1.1 nM of ferricrocin and 0–1.2 nM of ferrichrome in all podzol horizons, while Esse´n et al. (2006) detected higher concentrations (0.1–12 nM) of ferricrocin and (0.1–2.1 nM) of ferrichrome in the podzol horizons at four different locations in the north and south of Sweden. The findings of Esse´n et al. (2006) agreed with our results that the lower concentrations of hydroxamates were found in the lower B- and C-horizons. The differences in hydroxamates concentration between these previous studies and our findings may be due to: (1) the different geographical location where the samples were collected within Sweden, (2) the different analytical methods used in the HPLC– MS measurement and (3) the different methods used to obtain soil solution. Most previous studies are based on soil solution obtained by a centrifugation drainage technique (Giesler and Lundstro¨m, 1993). In contrast, we used different soil/liquid extraction methods to acquire the siderophores. Recently, Ali et al. (2011) extracted the siderophores from podzol soil from a location near to our sampling site at Bispga˚rden by two different methods, phosphate buffer and buffer-methanol mixture. They found small amounts of ferricrocin, while ferrichrome was not detected. The maximum concentration of dissolved ferricrocin was 3.74 nmol/kg soil that was obtained by the phosphate buffer extraction and found in the O-horizon. In contrast, we detected the highest concentration (1.1 nmol/kg dry soil (recalculated from pmol/g)) of dissolved ferricrocin using the water extraction method in the same horizon. The

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higher ferricrocin concentration that was detected by Ali et al. (2011) may be due to the different extraction methods used in these two studies. Most of the hydroxamate siderophores in soils were earlier suggested to be ferrichromes especially ferrichrome and ferricrocin (Moberg et al., 2003; Holmstro¨m et al., 2004; Esse´n et al., 2006; Winkelmann, 2007; Ali et al., 2011). In contrast, the present study detected a wide range of other fungal (coprogens and fusigen) and bacterial (ferrioxamines) trihydroxamates in the podzol soil. Therefore we suggest that while ferrichromes and ferrioxamines are more commonly found in the soil environment in low concentrations, coprogens and fusigen occur in higher concentrations. For instance, we detected Neocoprogen II concentration between 1.1 and 3.5 pmol/g dry soil; Neocoprogen I (0–14.4 pmol/g dry soil) and fusigen (0–38.8 pmol/ g dry soil). These variations of hydroxamates that we found in the soil horizons indicate that there is a high diversity of soil microorganisms that produce a wide range of siderophores. For example, ferrioxamines can be produced by Streptomycetes spp. (Das et al., 2007); ferrichromes by Aspergillus spp. (Charlang et al., 1981), Suillus variegates (Wallander and Wickman, 1999) and Microsporum spp. (Bentley et al., 1986); coprogens by Fusarium dimerum (Van der Helm and Winkelmann, 1994) and Epicoccum purpurascens (Frederick et al., 1981) and fusigen by Fusarium spp. (Van der Helm and Winkelmann, 1994) and Histoplasma capsulatum (Burt, 1982). Thus, taking into consideration our findings that coprogens and fusigen had the maximum concentrations in the soil horizons, it could indicate that microorganisms like Fusarium spp., E. purpurascens and H. capsulatum are the most abundant species in that soil. 4.2. Dissolved and adsorbed phases of hydroxamates As previously discussed, most of the hydroxamates were detected in the dissolved phase of the soil solution extract. In the present study, we found not only dissolved hydroxamates but also adsorbed hydroxamates with an average between 0 and 2 pmol/g dry soil for ferrioxamines; 0.3–2 pmol/g dry soil for ferrichromes; 0–32 pmol/g dry soil for fusigen and 0–13 pmol/g dry soil for coprogens. The presence of adsorbed hydroxamates could be dependent on physico-chemical properties of their functional group. Powell et al. (1980) demonstrated earlier that some reservoirs of siderophores are adsorbed to soil organic matter. In addition, Haselwandter et al. (2011) reported that the siderophores could be dissolved or adsorbed depending on their susceptibility to degradation. We found that each specific hydroxamate family has different behavior with regards to adsorption. The ferrichromes and ferrioxamines were found in a higher concentration in the dissolved phase than in the adsorbed phase. In comparison, the coprogens behaved in the opposite way; that is, they were more abundant in the adsorbed phase. These findings could be related to the different chemical structure of the specific hydroxamate functional group. The fusigen, ferrichromes, ferrioxamines and coprogens differ with regard to the characteristic bonds within the molecule that could form strong

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or weak bonds with the soil particles. For instance, three ester bonds are present in fusigen, six peptide bonds in ferrichromes, five peptide bonds in ferrioxamines, and one ester plus two peptide bonds in the coprogens (Winkelmann, 2007). The different behavior of the investigated hydroxamate families could also be explained by the wide range of lipophilicity. In addition to the different electrical charge of the respective siderophores, that will affect the mobility of the siderophores in the soil profile (Winkelmann, 2007). The main factor affecting the siderophores adsorption capacity is the effect of soil solution pH on the siderophore charge, rather than the effect of the charge of the mineral and soil particles. Some hydroxamates like DFO-B can remain adsorbed over a wide pH range (4.0–7.5) in accordance with their stable positive charge. However at higher pH values the adsorption decreased following a decline in its positive charge (Kraemer, 2004; Siebner-Freibach et al., 2004). This may explain the quite high stable concentration of adsorbed hydroxamates which we found in the soil horizons, in which the soil pH ranged between 4.4 and 5.4. There were also some differences in the individual types of hydroxamates with regards to their adsorption; that is, FO-B had lower adsorption compared to FO-D. This agrees with what Kraemer et al. (1999) and Kraemer (2004) found in that the electrostatic repulsion between the hydroxamates and the positively charged mineral surface results in lower adsorption of FO-B compared to FO-D at pH < 8. FO-B is a cationic species at pH < 8 due to protonation of the terminal amine group (pKa1 = 8.38), while FO-D is an acetyl derivative of FO-B which has no charge below pH 8.9. It has been suggested that the adsorption of hydroxamates in soil ecosystem are strongly influenced by their interactions with the solid phase like clay minerals that comprise a major part of the surface area in soils (Siebner-Freibach et al., 2004). On the other hand, some studies reported that hydroxamate siderophores are more commonly found in the dissolved phase in the soil. That is because they consist of strong cyclic hexapeptides that make them highly resistant to the environmental degradation by some enzymes produced by plants (i.e., hydrolases and proteases), which affect the life time of the siderophores (e.g. Hider and Kong, 2010). In addition, some hydroxamates are also resistant to degradation by soil microorganisms while others are not. For instance, pseudomonads isolated from soil are capable of degrading ferrichrome A (Warren and Neilands 1964), which may explain the very low concentration of ferrichrome A in our soil samples. 4.3. Siderophores in the presence of different minerals in the soil We found that the concentration of hydroxamates in the soil attached to the polished mineral surfaces was higher than that in the bulk soil. We also found that the dissolved hydroxamates had a higher concentration than the adsorbed hydroxamates for all investigated mineral types. However, the total dissolved and adsorbed hydroxamates showed a great variation between the different minerals. For example, the average concentration of total dissolved

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hydroxamates found on apatite, biotite and oligioclase was between 20 and 83; 42–107 and 18–36 pmol/g dry soil, respectively. In contrast, the average concentration of total adsorbed hydroxamates was between 35 and 64 pmol/g dry soil for apatite; 6–55 pmol/g dry soil for biotite and 0.009– 21 pmol/g dry soil for oligioclase. These findings could be dependent on the interaction between the siderophores and the specific mineral surfaces. For instance, when some trihydroxamate siderophores such as ferrioxamines react with iron containing minerals, only one Fe(III) center can be coordinated at a time (Cocozza et al., 2002) and the mineral dissolution reaction rates are controlled by the nature of the Fe(III)-siderophore complexes (Furrer and Stumm, 1986). Each polished mineral in our experiment also had a unique interaction with the dissolved and adsorbed hydroxamates in the different soil horizons. For instance, the maximum dissolved hydroxamates concentration was detected on biotite in the O-horizon and thereafter decreased with the depth of the soil. For oligioclase, the maximum concentration was found in O-horizon followed by the Bhorizon. However, the dissolved hydroxamates concentration on the apatite surface increased gradually with the depth of the soil until it reached maximum in the B-horizon. On the other hand, the maximum adsorbed hydroxamates were found on the surface of all the three different minerals in the E-horizon. The binding of strong complex formers like siderophores with cations on the mineral surface reduces the stability of the surface structure, thereby enhancing the weathering process (Ehrlich, 1998) and providing a highly efficient Fe acquisition system (Kraemer, 2004). There are a number of factors that influence the conformation and bonding of attached siderophores on mineral surfaces, i.e. siderophore architecture, charge, and hydrophobicity (Kraemer, 2004). There is also a limitation to the number of bonds that can form between the siderophore and a single Fe(III) ion in the inner coordination sphere at the mineral surface, which is why each mineral in our experiment had a unique behavior with regards to each siderophore type. Our findings regarding the interaction between the siderophores and the three different minerals can be considered new knowledge of how siderophore concentration and siderophore type can differ according to the presence of different minerals during the weathering processes under natural conditions. 4.4. The distribution of siderophores with regards to the soil horizons The PCA results verified that the soil horizons strongly influenced the distribution of adsorbed and dissolved hydroxamates. Our findings agreed with Bossier et al. (1988) and Nelson et al. (1988), who have suggested that the concentration of siderophores in soil depends strongly on the chemical, physical and biological properties of soil horizons. Three main reasons could explain the variety of siderophores distribution regarding the soil horizons: (a) chemical and mineralogical properties, (b) organic matter content and (c) the pH of the soil. The chemical and mineralogical properties of podzol soils change with depth, which

creates a number of different habitats for microorganisms throughout the soil profile (Fierer et al., 2003; LaMontagne et al., 2003; Rosling et al., 2003). The highest siderophore metabolic diversity was usually found in the O- and E-horizons as compared to B- and C-horizons. Hydroxamates concentration was also strongly correlated with the soil organic matter content, in which the low clay soils yielded almost twice as many hydroxamates as did high clay soils suggesting that adsorption might be an important determinant of their concentration in bulk soil solution (Powell et al., 1982). That can explain the highly adsorbed hydroxamates which were detected in the O- and E-horizons with regard to the high organic matter found in those horizons. However, the pH of the soil solution in our study was in the range of 4–5.5 and the majority of iron was soluble Fe(II); therefore, the microorganisms that produce siderophores at these pH values have a distinct advantage over non-siderophore producers. That is because of the extreme acid stability of the siderophore molecules that give them the ability to scavenge the needed iron from competing microorganisms and also protect themselves from the stress of Fe overdose. In these pH ranges, the structures of natural tri-hydroxamate siderophores allow the formation of intra molecular hydrogen bonds. These bonds are formed between the coordinating oxygen and the amide hydrogen, enhancing the stability of hydroxamate siderophores and resulting in their persistence in the soil environment (Matsumoto et al., 2001; Wittenwiler, 2007). 5. CONCLUSION A wide range of hydroxamates, both fungal (ferrichromes, coprogens and fusigen) and bacterial (ferrioxamines) were detected in a podzolic soil. These findings changed our previous knowledge that the ferrichromes are the predominant siderophore type in soil as indicated and suggested in earlier studies. For the first time coprogens and fusigen siderophores have been detected in podzolic soil and they were found in higher concentrations than ferrichromes and ferrioxamines. Each of the polished biotite, apatite and oligioclase minerals had a unique interaction with the dissolved and adsorbed hydroxamates in the different soil horizons, which makes the mineral type one of the factors affecting siderophore concentration and distribution in the natural environment. The concentration of hydroxamates in the soil attached to the polished mineral surfaces was greater than the concentration in the surrounding bulk soil indicating that the microbial communities attached to the mineral surfaces has a greater ability for siderophore production than the microorganisms in the bulk soil. The soil depth variability in concentration and composition of hydroxamate types in the bulk soil, in addition to the abundance and distribution of ferrichromes, ferrioxamines, fusigen and copregens on the different polished mineral surfaces in each horizon strongly suggest that our field experiment succeeded in describing how much the behavior of siderophores can differ with regard to the mineral type and the soil horizon characteristics. The next step is to gain greater insight into the siderophore mineral interactions in soils by investigating the microbial diversity in

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the bulk soil and soil attached to mineral surfaces, which could also have a major effect on the siderophore distribution. ACKNOWLEDGEMENTS We would like to thank Madelen Olofsson and Dan Bylund (Mittuniversitetet, Sundsvall, Sweden) for taking part in the field experiment setup and sampling. We would also like to thank the reviewers for their valuable comments and suggestions. We thank Anders Andersson (SciLifeLab, Stockholm, Sweden) and Hildred Crill (Stockholm University, Stockholm, Sweden) for English editing. The present study was supported by grants from “The Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS)” and the Faculty of Science, Stockholm University, Sweden.

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