Biogeochemical cycles of key elements in the paddy-rice rhizosphere: Microbial mechanisms and coupling processes

Rhizosphere 10 (2019) 100145

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Biogeochemical cycles of key elements in the paddy-rice rhizosphere: Microbial mechanisms and coupling processes Xiaomeng Weia,b, Zhenke Zhua, Liang Weia,b, Jinshui Wua, Tida Gea,

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Key Laboratory of Agro-ecological Processes in Subtropical Region & Changsha Research Station for Agricultural and Environmental Monitoring, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Hunan 410125, China b University of Chinese Academy of Sciences, Beijing 100049, China

A R T I C LE I N FO

A B S T R A C T

Keywords: Rhizosphere priming Nutrient availability Iron redox Microbial processes Coupling mechanism

Rice feeds more than 50% of the world’s population, 88% of which is planted in paddy fields. Paddy-rice rhizosphere is a unique habitat characterized by redox heterogeneity that is generated from radial O2 loss from roots and intensive water management, which allows the differentiation of microbial niches in the narrow rhizosphere and leads to strong couplings of functional processes. This review summarizes the biogeochemical processes of key elements (C, N, P, and Fe) in the rice rhizosphere and their coupling mechanisms. We emphasize the redox gradient in rice rhizosphere and the role of microorganisms in element cycling under altering redox conditions. We argue that C turnover and nutrient (N and P) availability are closely linked to each other, during which Fe reduction and oxidation play important roles. For further development in this field, we suggest further effort to reveal several key processes, including, the high resolution in situ distribution of biotic and abiotic factors, stoichiometric regulations on microbial processes, and the functions of key microbial guilds or species in element cycles.

1. Introduction

typically less than 5 mm from the root center (Ge et al., 2017a; Wei et al., 2018). Ge et al. (2017a) found that the expansion of the enzymatic rhizosphere was independent of rice growth in the first 30 days after transplanting. However, after further growth, the rhizosphere size increased for β-glucosidase activity but decreased for acid phosphomonoesterase activity (Wei et al., 2017). Paddy soils are largely anaerobic during the rice growing season because of continuous flooding (Kögel-Knabner et al., 2010). However, rice roots are well recognized by their capacity for radial O2 loss (ROL) and that they form a narrow aerobic or microaerobic zone in the rhizosphere (Wu et al., 2012). ROL leads to gradually decreasing redox from the root surface to the bulk soil, which substantially affects the biogeochemistry in the rice rhizosphere (Khan et al., 2016). As suggested by Faulwetter et al. (2009), the redox potential (Eh) near the root surface of wetland plants is about 500 mV, and it decreased to approximately −250 mV at 1–20 mm from the root surface. In the rice rhizosphere, the oxic zone is likely constrained in millimeter scale (Kögel-Knabner et al., 2010; Revsbech et al., 1999), depending on factors like ambient O2 concentration, root permeability, and the respiration of both roots and soil (Larsen et al., 2015; Armstrong and Armstrong, 2001). Larsen et al. (2015) reported the first in situ study of the O2 dynamic in the rice rhizosphere using planar optodes. They

Paddy rice encompasses 155 million hectares worldwide and is the main food source for more than 50% of the world’s population (http:// beta.irri.org/index.php/). The rhizosphere is one of the most dynamic habitats for element cycling due to carbon (C) input from roots (Kuzyakov and Blagodatskaya, 2015). The portion of photosynthesisderived C that is transported to underground and converted to soil organic C (SOC) through rhizodeposition ranges from 7.6% to 23.5% of rice biomass, depending on fertilization, water management, and rice growth stage (Atere et al., 2017; Atere et al., 2018a; Atere et al., 2018b, Ge et al., 2015). The C is mainly sequestrated in the rhizosphere and only a small part diffuses to the bulk soil (Atere et al., 2017; Atere et al., 2018). Nitrogen (N) limitation strongly decreases the rate of rhizodeposition (root exudates or dead root cells, Atere et al., 2017; Ge et al., 2015; Zhao et al., 2018a), while a higher rhizodeposition rate under phosphorus (P)-poor conditions was observed, compared to the P-fertilized treatment (Atere et al., 2018). The rates of microbial processes in the rhizosphere are dozens to hundreds of times higher than the bulk soil, as indicated by microbial growth, soil respiration, mineralization potential, and enzyme activities (Kuzyakov and Blagodatskaya, 2015). When referred by enzyme activities, the size of the rice rhizosphere is

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Corresponding author. E-mail address: [email protected] (T. Ge).

https://doi.org/10.1016/j.rhisph.2019.100145 Received 10 December 2018; Received in revised form 4 February 2019; Accepted 8 February 2019 Available online 10 February 2019 2452-2198/ © 2019 Elsevier B.V. All rights reserved.

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nutrient availability (Luo et al., 2018). However, the mean residue time of rice rhizodeposit C was reported to be 66.2 ± 0.9 days (Zhu et al., 2017a), which is six times longer than the that of upland crops (Zang et al., 2017). The microbial necromass has been shown to be the primary constituent of SOC (Kindler et al., 2006; Schweigert al., 2015). In Yuan et al. (2016), 13C was detected in the phospholipid fatty acid of rhizosphere microorganisms only 6 h after the rice plants were labeled with 13C dioxide (13CO2). The rapid incorporation of rhizodeposit C into microbial biomass may explain the high levels of C sequestration in paddy soil (Liu et al., 2019). Despite flooding, fungi show the highest capacity for assimilating rhizodeposits, followed by bacteria and actinomycetes (Ge et al., 2017b; Yuan et al., 2016). Many previous studies have found that the mineralization of SOC increased with root C input (i.e., positive rhizosphere priming) in upland soils (e.g., Bengtson et al., 2012; Kumar et al., 2016). However, the stimulation of root exudate C on SOC decomposition in paddy soil is much slighter than in upland soil, resulting in weaker positive or even negative rhizosphere priming (Ge et al., 2012; Qiu et al., 2017; Zhu et al., 2018). Atmospheric CO2 concentration and temperature increases have been improving the plant photosynthesis and rhizodeposition (Asseng et al., 2004; Ikawa et al., 2018; Li et al., 2018a), which indicates the rising significant role of rhizosphere priming on the global C cycle. Lower decomposition rates of rhizodeposition C and the weaker priming effect on SOC in paddy soil compared to upland soil would make it more important to sequester more atmospheric C under global climate change than the current situation. Direct assimilation of CO2 by soil microorganisms is another mode of C sequestration in paddy soil (Fig. 1, Yuan et al., 2012). The CO2 fixation rate of paddy soil in the plough layer is 86–166 mg C m−2 d−1 (Jian et al., 2016), which is 2–10 times higher than that of upland soil (Ge et al., 2013; Yuan et al., 2012). Microbial CO2 assimilation is dominated by phototropic processes (Yuan et al., 2012). Thus, the abundance and activity of CO2-fixing bacteria decreased with soil

found intense leakage of O2 around root tips and younger roots. The results were similar to those using the traditional method (Wang et al., 2013). The redox gradient in the rice rhizosphere allows the inhibition of various microbial functional guilds with niche differentiation, which drives the biogeochemical cycles of key elements, specifically, C, N, P, and iron (Fe) (Kögel-Knabner et al., 2010). Reddish-brown precipitates of Fe and manganese oxides on the root surface and in the rhizosphere are created by the altering redox and is termed “iron plaque” (Khan et al., 2016). The formation and collapse of iron plaque interact with the transformation of C and nutrients and of significant implication on the biogeochemical cycles in the rice rhizosphere. This review focuses on the microbial mechanisms of C and nutrient turnover in the rice rhizosphere. We first summarize the biogeochemical processes of C, N, P, and Fe. Then, we review the coupling cycles of these elements. The relationship between rhizosphere priming and nutrient availability is discussed, as well as the root C effect on the N and P cycles, during which Fe plays a key role. Finally, we provide an outlook for future research.

2. Biogeochemical processes of key elements in the rice rhizosphere 2.1. Carbon turnover Soil C loss is universal in arable land as a result of farming (Cotching, 2018). However, paddy ecosystems have been considered as carbon sinks during the past decades. They have significantly higher SOC content in the top soil than upland arable field, orchard, forest, scrub, and grass ecosystems (Zhao et al., 1997; Wu, 2011). This is partly due to the relatively slow decomposition of both fresh and native C under anoxic conditions (Boye et al., 2017). Rhizodeposits are the major C input to paddy fields during rice growth (Fig. 1, Ge et al., 2015; Lu et al., 2002). The stabilization of rice rhizodeposition is affected by

Fig. 1. Schematic overview of the coupling cycles of C, N, P, and Fe in rice rhizosphere. Red arrows correspond to the C-cycling processes including the rhizosphere priming effect (PE) on the mineralization of soil organic C (SOC), CO2 fixation, and CH4 oxidization; blue arrows correspond to the N-cycling processes including N2 fixation, nitrification, denitrification, and organic N mineralization; green arrows correspond to the P-cycling processes inorganic P (Pi) dissolution and organic P (Po) mineralization. AMO: aerobic methane oxidization; ANMO: anaerobic methane oxidization; Feammox: NH3 oxidation pathway coupled with the reduction of ferric minerals; FeRB: Fe reducing bacteria; Fe oxidizing bacteria; PSB: P-solubilizing bacteria; Phos: phosphatases.

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Phosphorus is considerably abundant in many soils. However, only a small portion is available for plants, as most orthophosphates are strongly bound to soil particles (Richardson and Simpson, 2011). This is even worse for oxisols in tropical and subtropical areas, which are the main rice-producing regions. Microorganisms drive the mobilization of both inorganic and organic P (Sun et al., 2018). P-solubilizing bacteria (PSB), including Burkholderia, Bacillus, Gluconacetobacter, Sphingomonas, were isolated from the rice rhizosphere (Loganathan and Nair, 2003; Panhwar et al., 2014; Panhwar et al., 2011). Abundant organic acids are produced by PSB, resulting in the release of phosphate from Pcontaining minerals (Fig. 1, Richardson and Simpson, 2011). Organic P accounts for 30–80% of the total P pool (Linquist et al., 2011; Yin and Liang, 2013), but it is only available after mineralized by phosphatases (Richardson, 2011). Phosphomonoesterases catalyze the mineralization of orthophosphate monoesters (Fig. 1, Nannipieri et al., 2011), which are the most common form of organic P in soil (Condron et al., 2005). Among the phosphatases, alkaline phosphomonoesterase is exclusively produced by microorganisms (Nannipieri et al., 2011, 2018) and is widespread across the bacteria kingdom, and has also been detected in fungi and archaea (Ragot et al., 2015). Three homologous genes code the alkaline phosphomonoesterases, i.e., phoA, phoD, and phoX (Gomez and Ingram, 1995). Compared to phoA and phoX, the expression of phoD is critically induced by P starvation (Apel et al., 2007). Studies suggest that phoD has potential to improve soil P availability under P poor conditions (Fraser et al., 2015; Hu et al., 2018; Sun et al., 2018). In rice rhizosphere, rare taxa of phoD harboring microorganisms may contribute to the P mineralization than the dominants (Wei et al., 2019). Inoculation of arbuscular mycorrhizal fungi would increase rice growth and yield through enhancing P uptake (Hoseinzade et al., 2016). However, different studies have found different results (Herdler et al., 2008), perhaps due to the differences in soil P availability (Kobae et al., 2016). Taxonomic differences in the tested mycorrhiza may also lead to discrepancies, as only a few mycorrhizal species are able to colonize rice roots and survive under flooding conditions (Paszkowski et al., 2002; Gutjahr et al., 2009).

depth; the CO2-fixation ability was 100 times stronger in the top 1 cm than 5 cm deeper (Ge et al., 2016; Wu et al., 2014). While chemoautotrophic CO2-fixation is more than 10 times lower than the phototropic pathway (Long et al., 2015; Jian et al., 2016), it still potentially contributes to microbial C sequestration because soil is highly lightproof. CO2-assimilating genes, including cbbLG, cbbLR, cbbM, alcB, oorA, and accA, are significantly more abundant in the rhizosphere than in bulk soil (Xiao et al., 2014), indicating that the rhizosphere has greater potential for C fixation. However, a high functional gene copy number does not always lead to high CO2-fixing rate (Ge et al., 2016; Zhao et al., 2018b), indicating that the CO2 fixation capacity of soil is controlled by the abundance of autotrophic microorganisms as well as their community composition (Long et al., 2015). Despite few specific studies on the rice rhizosphere, microbial CO2 fixation has been found to be affected by environmental factors and anthropogenic disturbance, including pH (Long et al., 2015), soil type (Ge et al., 2013; Long et al., 2015), land use (Lynn et al., 2017; Yuan et al., 2013; Yuan et al., 2015; Wu et al., 2017a), tillage (Ge et al., 2016), fertilization (Huang et al., 2018; Wu et al., 2017b), and irrigation (Wu et al., 2017b). Microbialderived organics such as cell wall fragments, exoenzymes, and osmolytes significantly contribute to SOC (Liang et al., 2017; Schimel et al., 2007). The mineralization of microbial C is much slower than rhizodeposition and rice residues (Zhu et al., 2017a). Approximately 90% of the organic C derived from C fixation of autotrophic microorganisms was stabilized in the paddy soil after 300 days of incubation (Zhu et al., 2017b). This magnitude was three to five times higher than that of the C in plant materials. The results suggest that microbial C is more persistent than plant-derived C in long-term decomposition. The C-use efficiency of heterotrophic microorganisms in soil never reached 0.6 (Sinsabaugh et al., 2013). That means more than 40% of plant-derived C is consumed for energy production when converted to microbial biomass. Therefore, the direct incorporation of atmospheric C into microbial biomass might be the most efficient pathway for soil C sequestration. 2.2. Nitrogen and phosphorus cycles

2.3. Iron redox Nitrogen cycling processes in soil mainly include nitrification, denitrification, organic N mineralization, and N2 fixation (Fig. 1, Canfield et al., 2010). The former two lead to N loss (Long et al., 2018a), while the latter two increase the availability of N (Zhu, 1989; Drinkwater and Snapp, 2007). Microorganisms involved in the N cycle occupy different niches in paddy soil according to the redox gradient derived from ROL (Chen et al., 2008a; Fujii et al., 2010; Wang et al., 2012; Hu et al., 2017). Per Arth and Frenzel (2000), nitrification occurred in the first 2 cm from the root surface, while denitrification occurred at 1.5–5 cm. Among the ammonia (NH3)-oxidizing prokaryotes, NH3-oxidizing archaea dominate the rice rhizosphere and are assumed to be more sensitive to C input than NH3-oxidizing bacteria (Chen et al., 2008a; Wei et al., 2017; Li, Chapman et al., 2018b). Rice prefers ammonium (NH4+) to nitrate (NO3−) as a N source (Sasakawa and Yamamoto, 1978). NH4+-based fertilizers like urea are universally applied in paddy fields. Thus, the NO3− content in paddy soil is generally low and the activity of denitrification is constrained by the NO3− production from nitrification. Nitrification and denitrification led to strong gaseous N loss (N2, NO, and N2O) in paddy soil, which accounts for 13% of the total N application (Zhang et al., 2018). NH4+ concentration decreases with decreasing distance from the rice zone due to root uptake (Li et al., 2007). The low NH4+-N concentration may benefit the colonization of diazotroph and lead to a high abundance of N2-fixing bacteria in the rhizosphere (Ayuni et al., 2015; Yoon et al., 2015). Biological N2 fixation accounts for 16–21% of rice N in non-fertilized soil (Zhu, 1989). More than 40% of crop N is derived from the mineralization of organic N even in fertilized soil (Drinkwater et al., 2007). The process is potentially substantial for plant N acquisition. However, little is known regarding the organic N turnover in the rice rhizosphere.

Rice is mainly planted in weathered soil with high Fe content. A significant character of the rice rhizosphere is the formation of iron plaque (Khan et al., 2016). Depending on its amount, iron plaque reduces or increases the nutrient supply to the roots (Khan et al., 2016; Zhang et al., 1999), further affecting rice growth and yield. Chemical oxidation by O2 is considered as the main driver for iron plaque formation (Zhang et al., 2012). However, microorganisms also contribute to the oxidation of Fe(II) in the rice rhizosphere (Fig. 1, Chen et al., 2017; Weber et al., 2006). Fe-oxidizing bacteria (FeOB) require microaerobic conditions, with O2 concentration ranging from 3 to 10 μm (Dubinina and Sorokina, 2014). This niche coincides with 0.5–1.5 mm from the rice root surface (Han et al., 2016). Neubauer et al. (2002; 2007) observed the Fe2+ oxidation in the rhizosphere of wetland plants and concluded that FeOB contributed to 18–62% of the total Fe2+ oxidation. However, information about the in-situ colonization of FeOB in the rice rhizosphere is still lacking. Previous research found that iron plaque was only visible in submerged soil rather than in well drained treatments (Chen et al., 2008b). The results suggest the importance of Fe-reducing for iron plaque formation. Fe reduction in the rhizosphere has been considered to be mainly controlled by chemical processes for a long time (Weiss et al., 2004), but more recently it has been accepted to be primarily driven by microorganisms (Fig. 1, Luo et al., 2018; Zecchin et al., 2017). Geobacteria and Shewanella are the most identified Fereducing bacteria (FeRB) (Weber et al., 2006), which are frequently reported in the rice rhizosphere (Wang et al., 2009; Zecchin et al., 2017). The FeRB account for 12% of total bacteria in the rhizosphere, but only < 1% in the bulk soil (Weiss et al., 2003). O2 strongly damages the activity of Fe reductase (Schroder et al., 2003). However, more 3

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abundant FeRB were found in the rhizosphere than in the bulk soil (Chen et al., 2008b), leading to an Fe reduction rate two times higher than in non-rhizosphere soil (Weiss et al., 2004), probably because of the high Fe(III) content on the root surface (Tian et al., 2015). In-situ study on the distribution of Fe minerals, FeRB, and FeOB at the microscale may help to reveal the microbial mechanism of the Fe cycle in the rice rhizosphere.

N mineralization and plant N uptake. N fertilizer application, which significantly increased rice root biomass and rhizodeposits through stimulating the plant growth, resulted in preferential microbial utilization of plant-derived C (negative priming) (Kuzyakov and Xu, 2013). The mechanism might be primarily through regulating the microbial biomass stoichiometric ratio and extracellular enzyme activity (Kumar et al., 2016; Zhu et al., 2018).

3. Coupling processes of carbon, nitrogen, and phosphorus

3.2. Carbon effect on nitrogen cycle

3.1. Rhizosphere priming and nutrient availability

Root exudate is the primary C input in the rhizosphere. It shapes the N cycle in at least two ways: first, supply energy and stimulate the metabolism of heterotrophic microorganisms; second, work as inhibitor or promoter for microorganisms involved in N transformations (Coskun et al., 2017). Denitrification depends on the availability of C resources (Chen et al., 2018; Starr and Gillham, 1993; Pan et al., 2017). Elevated CO2 levels have been shown to increase the activity of denitrifiers in the rhizosphere of upland plants, due to the increasing release of photosynthetic C from the roots (Smart et al., 1997; Carnol et al., 2002). However, despite very few relevant reports, CO2 enrichment was found to decrease the denitrification rate in the rhizosphere of rice (Han et al., 2006; Wang et al., 2007). Yue et al. (2007) observed increased populations of denitrifiers by elevated CO2, but only during the late ricegrowing season (drained). This is most likely because of NO3− limitation under flooding conditions. Moreover, high C input stimulates the growth of rhizosphere microorganisms universally, which may restrict denitrifier activity through strong competition (Wang et al., 2007). A biological denitrification inhibitor was recently detected in the root exudate of Fallopia spp. (Bardon et al., 2014), but it has not been found in root exudate or tissues of rice (Coskun et al., 2017). Biological N2 fixation is also affected by root C input. Higher N2 fixation rates have been observed during early rice growth when the root exudation is most active (Yoshida and Ancajas, 1973; Ladha et al., 1986) and in the rhizosphere of cultivars with large root systems (Hirota et al., 1978). Additionally, increased abundance and activity of diazotrophs were observed in free-air CO2-enrichment experiments (Guo et al., 2015; Hoque et al., 2001). Chemoattractants in root exudates recruit Cyanobacteria like Nostoc to the surface and interspace of rice roots, and form paranodules with higher N2-fixing rate than free-living Cyanobacteria (Yoneyama et al., 2017; Nilsson et al., 2002). 1,9-decanediol, a new biological nitrification inhibiting compound, was identified in the root exudate of rice and shown to reduce N loss and increase plant N use efficiency (Rosolem et al., 2017; Sun et al., 2016). However, the information is still limited. Another coupling process of C and N in the rice rhizosphere that should not be neglected is the N cycle involved in methane (CH4) oxidation (Fig. 1). 61–83% of rice root exudate C in the rhizosphere is converted to CH4 (Aulakh et al., 2000), 60–80% of which is oxidized by methanotrophs before being emitted to the atmosphere (Singh et al., 2010). The nitrogenase-coding gene (nifH) was detected in both type I and type II aerobic methanotrophs (Auman et al., 2001). N2 fixed by methanotrophs was transferred to rice shoots at a high efficiency and was estimated to be as much as 12% of plant N (Bao et al., 2014). Type II methanotrophs including Methylosinus and Methylocystis are suggested to be the main players for CH4-dependent N2 fixation (Auman et al., 2001). Their contribution might prevail over the heterotrophic diazotrophs under submerged conditions (Yoneyama et al., 2017). CH4 and NH3-oxidizing bacteria share similar substrates, homologous key enzymes (CH4 monooxygenase vs. NH3 monooxygenase), and the same phospholipid fatty acid cytomembranes (16:0 and 16:1) (Jia and Cai, 2003). CH4 oxidation was performed by NH3 oxidizers in pure cultures and rice rhizosphere soil in lab experiments (Bodelier and Frenzel, 1999; Wang et al., 2016; Ward, 1987). However, there is still no direct evidence for CH4 oxidation mediated by NH3-oxidizing nitrifiers in the field. Denitrifying anaerobic CH4 oxidation (DAMO) has created great interest since its discovery (Raghoebarsing et al., 2006). Both NO3−-

Soil organic matter (SOM) is the predominant source of nutrients required for rice growth, but the availability of these nutrients depends on the transformations mediated by microbial turnover. This is strongly affected by rhizodeposition, as labile C promotes microbial activity and change their C-use strategy (rhizosphere priming) (Paterson, 2003; Cheng and Kuzyakov, 2005; Yao et al., 2012). The extent to which positive/negative priming occurs results in increased/decreased rates of gross C, N, and P mineralization, which are likely a function of relative substrate quality, mineral nutrient availability, and microbial community composition (Cheng et al., 2001; Fontaine et al., 2003; Kuzyakov, 2010; Dijkstra et al., 2013). However, the extent and the actual mechanisms are virtually unknown, limiting our ability to predict an important driver of C, N, P, and other nutrient element cycling in soils (Cheng and Kuzyakov, 2005; Ostle et al., 2009; Shibu et al., 2012; Finzi et al., 2015). Nutrient availability in rice-soil systems, especially the rhizosphere, affects microbial activity and SOM decomposition (Fig. 1). The direction and magnitude of rhizosphere priming have been related to soil nutrient availability (Dijkstra et al., 2013; Zhu et al., 2018). In soils with oligotrophic conditions (low nutrient availability), microorganisms meet their nutrient demands by stimulating enzyme synthesis to maximize SOM mineralization (Phillips et al., 2011). This accelerates SOM decomposition, resulting in a positive priming effect. Alternatively, in eutrophic conditions (rich nutrient availability), microorganisms will switch from decomposing SOM to utilize newly labile C and mineral N, resulting in a negative priming effect (Fig. 1, Cheng et al., 2014; Dijkstra et al., 2013, Guenet et al., 2010). Inhibition of rhizodeposition on the decomposition of SOC is frequently observed in paddy soil even under nutrient limitation (Ge et al., 2012). However, N fertilization leads to greater negative priming or less positive priming, which indicates reduced consumption of SOC as compared to the unfertilized soil (Zhu et al., 2018). Priming of SOM decomposition may considerably affect soil N supply and feedback to plant N availability (Fig. 1, Hu et al., 2001). For rhizosphere soils, the increased mobilization of N from SOM is ecologically significant, despite depletion of mineral N pools initially, because N has been transferred from a stable form (SOM) to a more labile one (microbial biomass) (Patra et al., 2010). In the context of rhizosphere processes, C flow from the roots may stimulate N mineralization, exploiting the complementary resource limitations of plants and microbial communities (Paterson, 2003). Rhizodeposits might provide a C-rich substrate (Suzuki et al., 2009), causing N limitation for soil microbes that begin producing N-degrading enzymes to obtain N from SOM (Chen et al., 2014a). However, Finzi et al. (2015) suggested that the largest losses of SOC occur when the C:N ratio of exudates is < 7, because of an increase in the efficiency of SOM decomposition, whereas SOC losses are dampened when the C:N is > 7. In addition, there are positive correlations between gross N mineralization and SOM decomposition (Harrison-Kirk et al., 2014; Liu et al., 2018), providing strong evidence that both microbial demand for N and exudate-induced shifts in microbial communities accelerate nutrient release from SOM (Chen et al., 2014a). Moreover, Bhattacharyya et al. (2016) found that an elevated CO2-induced increase in higher diversity and abundance of C and N decomposition bacteria, which are potential to increase the soil 4

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and nitrite (NO2−)-dependent DAMO processes have been detected in paddy soils (Ding et al., 2016; Shen et al., 2014; Xu et al., 2018), and their overall consumption rate of CH4 was estimated to be 250 nmol g−1 d−1 (Ding et al., 2016) or 0.14 g m−2 year−1 (Shen et al., 2014) through in situ experiments.

stabilize SOM against biodegradation. Therefore, understanding the efficiency and mechanism of the C stabilized by Fe minerals in the rhizosphere is essential to predict the potential of C sequestration in paddy soils. Most root exudates and plant- or microbe-derived dissolved organic C can bind to reactive Fe minerals by adsorption or coprecipitation (Chen et al., 2014b). Adsorption of organic compounds onto mineral surfaces is an important and well-documented process for SOM stabilization (Kaiser et al., 2007; Mikutta et al., 2007). Moreover, coprecipitation of organic compounds with minerals is a common process in many environments, especially in paddy soils, due to changes in pH, O2 gradient, or redox potential (Chen et al., 2014b; Katoh et al., 2004). In addition, poorly crystalized Fe minerals are easily transformed into more thermodynamically stable and more crystalized minerals, catalyzed by dissimilatory FeBR, Fe(II), or O2 in the rice rhizosphere. This leads to the organic C being adsorbed to or coprecipitated with secondary minerals during the transformation process (Shimizu et al., 2016; Liu et al., 2016); thus, the coprecipitated organic C is bound to the soil and less likely to decompose (Cooper et al., 2016). The Fe oxides or their secondary minerals bind organic compounds through their high specific surface area, variably charged surface hydroxyl groups, and various bonding sites (Chorover et al., 2001; Keiluweit et al., 2015; Mikutta et al., 2007). Such Fe mineral–organic associations inhibit microbial and enzymatic access and are quantitatively the most important mechanism protecting C from microbial utilization for longterm C sequestration (Fig. 1, Lehmann and Kleber, 2015; Mikutta et al., 2006).

3.3. Carbon effect on phosphorous mobilization Modelling and experimental evidences have suggested that P limitation for plant growth is derived from the P supply to the root surface, rather than the P uptake capacity of the root (Richardson et al., 2009). Root exudation is an important strategy for plants to increase access to P (Fig. 1, Tawaraya et al., 1998; Zou et al., 2018). Organic acids are released to the rhizosphere by many species when facing P starvation, including rice (Bhattacharyya et al., 2013; Li et al., 2006; Tawaraya et al., 2018). These acids significantly decrease the rhizosphere pH (Kirk et al., 1999; Zhang, Huang, Ye et al., 2009) and change the surface characteristics of soil minerals (Bhattacharyya and Datta, 2004), which extract P from the precipitated and adsorbed forms (Bhattacharyya et al., 2013). In addition, root exudation regulates the activity of pqq promoter in phosphate-solubilizing bacteria (Luduena et al., 2017). A previous study revealed different utilization rates of root C by solubilizing microorganisms under low and high P conditions in the rice rhizosphere, which indicated an intricate microbial mechanism of the C and P coupling process (Long et al., 2018b). The quality and quantity of soil C resource strongly affects the phoD that harbors microbial community and phosphatase activities (Heuck et al., 2015; Loeppmann et al., 2016; Luo et al., 2017). “Rhizosphere effect” leads to significantly higher activity of alkaline phosphatases in the vicinity of rice roots (Ge et al., 2017a; Li et al., 2008), probably due to the stimulation of root exudate C on microorganisms responding to organic P mineralization (Spohn et al., 2013; Yuan et al., 2018).

4.2. Anaerobic ammonia oxidation coupled with Fe(III) Reduction A unique NH3 oxidation pathway coupled with the reduction of ferric minerals (Feammox) when O2 is limited has been investigated in recent years (Fig. 1, Clément et al., 2005; Park et al., 2008). This process is critical for the N cycle in submerged soils and sediments (Clément et al., 2005; Huang et al., 2016) and was first detected in paddy soil by Ding et al. (2014). At least three different Feammox pathways are conducted by different microorganisms, generating NO2−, NO3−, or N2 as the terminal product (Clément et al., 2005; Yang et al., 2012). Direct N2 production is the main pathway of Feammox (Ding et al., 2014; Yang et al., 2012). Feammox leads to a gas N loss of 7.8−61 kg N ha−1 year−1 in paddy soil as estimated by N2 emission (Ding et al., 2014). This magnitude is comparable to the contribution of amminox and denitrification (Ju et al., 2009; Zhu et al., 2011). The Feammox rate is strongly dependent on the reduction rate of Fe3+ (Ding et al., 2014; Zhou et al., 2016). As described in Section 2.3, due to the lack of substrate in the bulk soil, the abundance and activity of Fereducing microorganism are significantly high in the rhizosphere (Weiss et al., 2004; Tian et al., 2015). Therefore, Feammox in paddy soil is speculated to primarily occur close to the rice root. Studies have suggested that the Feammox reaction is conducted by dissimilatory Fereducing microorganisms (Clément et al., 2005; Shuai and Jaffe, 2019), and the Fe reduction rate is stimulated by NH4+-based fertilization in the rice rhizosphere (Benckiser et al., 1984).

4. Role of iron in the carbon, nitrogen, and phosphorous cycles 4.1. Mineral protection of soil organic matter The rice rhizosphere is an important microbial hotspot in paddy soils (Kuzyakov et al., 2017). Rhizodeposits (root exudates or dead root cells) supply a sufficient C source for microbes and contribute to SOC assimilation (Ge et al., 2015; Lu et al., 2002). This may be due to fast uptake and assimilation of these organic compounds by microorganisms (Kuzyakov et al., 2002) and stabilization by sorption to reactive mineral phases, such as hydrous Fe oxides (Sodano et al., 2016). The active Fe minerals are prevalent in the rhizosphere and mainly distributed in the iron plaque on the roots and poorly crystalized minerals in the rhizosphere soil (Kusunoki et al., 2015; Vogelsang et al., 2016). The dissolved ferrous Fe produced by reductive dissolution of ferric Fe minerals represent two distinct types of mineral phases: (i) ferric iron plaques around younger rice roots, and (ii) secondary ferrous Fe minerals in the rhizosphere soil and around older rice roots. The formation of active Fe minerals is caused by the transport of O2 by plant aerenchyma (Nanzyo et al., 2010; Kusunoki et al., 2015), or Fe-oxidizing bacteria, making microsites around rice roots as hotspots for Fe and C cycling (Conrad, 2007). The active Fe minerals serve as important sorbents for organic C in the rhizosphere (Kaiser and Guggenberger, 2000; Keiluweit et al., 2015; Zhang et al., 2013). Mineral-bound organic C is relatively stable and regulates long-term stability of SOC (Mikutta et al., 2006; Mikutta et al., 2014). The quantity and quality of native SOC as well as fresh rhizodeposit C have fundamental importance in rhizosphere C storage (Kalbitz et al., 2008). It is evidenced that microbial accessibility to substrates, rather than the chemical recalcitrance of organic matter, determines the persistence of C in soils (Lehmann and Kleber, 2015; Schmidt et al., 2011). Microbial accessibility is believed to be substantial in its effects on organic compounds associated with minerals to

4.3. Iron redox effect on phosphorous availability P availability is limited by the affinity to Fe (hydro) oxides in highly weathered tropical and subtropical soil (Richardson et al., 2009; Zhang et al., 1999). Ferrous Fe dissolves better in soil solution than ferric minerals (Zhang et al., 2012). Therefore, the associated P is released when Fe reduction occurs under anoxic conditions, while it is strongly fixed under oxic conditions (Fig. 1, Maranguit et al., 2017). The rhizosphere is the key zone where P-dynamic coupling with Fe redox occurs. The greatest interest has been focused on the role of iron plaque in rice P uptake. According to Hansel et al. (2001), ferrihydrite is the main compound in iron plaque, of which the P adsorption potential is as much as 45,045 μg P g−1 (Zhao et al., 2006). Thus, iron plaque is 5

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Fig. 2. Framework for suggested future research on microbial mechanisms driving the biogeochemical cycles in the rice rhizosphere.

between rhizosphere and bulk soil in most cases, while they have ignored the heterogeneity of chemical and microbial properties at a microscale within the rhizosphere. Microorganisms are the main drivers of all the processes, however, studies about the relevant mechanisms are just beginning. In the future, studies should focus on the following issues (Fig. 2):

believed to be a barrier for plant uptake of P (Greipsson, 1995; Liu et al., 2004). Further studies indicate that the blocking seems to primarily work when the iron plaque is overabundant (Xu et al., 2009). While in other cases, the iron plaque acts as a medium for rice P uptake, which significantly improves the P availability on the root surface (Liang et al., 2006; Zhang et al., 1999). The P concentration in iron plaque is significantly higher than in the bulk soil (Khan et al., 2016). Enhanced P uptake is observed with increasing iron plaque in both solution cultivation and pot experiments (Liang et al., 2006; Xu et al., 2009; Zhang et al., 1999). More iron plaque is formed when P is deficient in the rhizosphere, probably to increase the root capacity for phosphate trapping (Liu et al., 2004). The P turnover involved in Fe redox has long been recognized as chemically derived (Li et al., 2007; Zhang et al., 2003). However, the role of microorganisms has emerged recently (Maranguit et al., 2017; Zhang et al., 2014). ROL was suggested to only account for 1/9 of the total oxidizing capacity of rice roots (Armstrong, 1967). FeOB may contribute substantially to the remaining drivers for iron plaque formation (Chen et al., 2008b), and therefore, the sequestration of P. As ROL decreases after the heading stage, the iron plaque gradually collapses, likely because of the reduction of Fe3+ by FeRB (Khan et al., 2016). It has been reported that the activation and turnover of Fe3+-fixed P is enhanced by Fe-reducing bacteria (Zhang et al., 2014). However, the microbial regulation of P transformation in the soil-iron plaque-root system is still unclear.

1. High-resolution studies on the gradient of environmental factors like O2, pH, rhizodeposition C, N, P, and Fe, as well as the biotic properties, like microbial composition, enzyme activities, and soil and root respiration. Specifically, attention should be paid on the changes in O2 concentration, C decomposition, and nutrient availability under dry-rewetting cycling. The development of non-destructive in-situ methods (e.g., planar optodes, diffusion gradient transformation, soil zymography, and fluorescence in situ hybridization) provides an opportunity to explore the heterogenous microenvironment of the rice rhizosphere. 2. Stoichiometric mechanisms underlying the coupling cycles of key elements, especially C, N, and P. All bio-reactions are controlled by the stoichiometric balance between substrates and organisms, which are affected by root C input and nutrient uptake. Investigating the relationships between the stoichiometry of soil available resources, microbial biomass, and enzyme activities is a powerful way to reveal the interaction of different functional processes. This may also help to understand the control of N and P runoff from paddy fields, which largely contributes to the nutrient loss and eutrophication due to frequent drainage. 3. Linking microbial community composition to ecological function. Isotopic labeling technology coupled with microbiome methods like DNA-SIP, RNA-SIP, and SIP metagenomics are useful to reveal the microorganisms involved in the turnover of certain substrates. Combined with metabolomics and proteomics, it is possible to trace

5. Prospective Overall, our knowledge of the biogeochemical cycles in the rice rhizosphere is limited. Most studies have focused on a single element or process, despite the numerous interactions. The role of Fe redox in C sequestration and nutrient immobilization is scarcely understood. Previous studies have only provided rough profiles of the differences 6

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the element flow at molecular and microbial species level, and therefore to look deeply into microbially-mediated processes, especially unspecific processes like priming. 4. High-throughput sequencing-based microbiome methods coupled with culturomics. Revealing the microbial contribution to the element cycles at the community and pure culture levels. Building the microbial resource bank and artificial assembly of the core microbiome in the rice rhizosphere.

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