Abundance, Diversity, and Structure of Geobacteraceae Community in Paddy Soil Under Long-Term Fertilization Practices

Applied Soil Ecology 153 (2020) 103577 Contents lists available at ScienceDirect Applied Soil Ecology journal homepage: www.elsevier.com/locate/apsoil Abundance, diversity, and structure of Geobacteraceae community in paddy soil under long-term fertilization practices T ⁎ Xiaomin Lia,b, Longjun Dinga, , Xiaoming Lia, Yongguan Zhua,b,c a State Key Lab of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China b University of Chinese Academy of Sciences, Beijing 100049, China c Key Lab of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China ARTICLE INFO ABSTRACT Keywords: Geobacteraceae is an important dissimilatory Fe(III) reducer that affects the cycles of multiple elements. Geobacteraceae However, the way in which different long-term fertilization regimes influence the Geobacteraceae community in Paddy soil paddy soils remains unknown. Therefore, the objective of this study was to explore the responses of Fertilization Geobacteraceae community in paddy soil to long-term chemical (nitrogen, phosphorus, and potassium) and/or Soil properties organic (manure) fertilization practices. Illumina sequencing results showed that the species richness and di- Iron reduction versity of Geobacteraceae community were not significantly changed by fertilizer treatments. Geobacteraceae in the treatments consisted of Geobacter (accounting for 90%–95% of total reads) and Geothermobacter genera (5%–10%), and all fertilizer treatments induced a significant (P < 0.05) decline in Geobacter and a marked enrichment of Geothermobacter. The taxonomic (based on Bray-Curtis distance) and phylogenetic structures (weighted-UniFrac distance) of the Geobacteraceae communities in all fertilizer treatments were clearly different from those in the non-fertilizer treatment; however, there were no significant changes among the different fertilization treatments. The variations in the Geobacteraceae community induced by long-term fertilization were mainly determined by changes in soil pH, total carbon, and total nitrogen. These findings provide an insight into the biogeochemistry of paddy soils and pave the way for harnessing the microbiome to improve soil fertility and environmental quality. 1. Introduction marine and lake sediments as well as paddy soils (Lovley et al., 2004; Bond et al., 2002; Fan et al., 2018; Yuan et al., 2016) and play a con- Dissimilatory iron reduction is a process used by microorganisms to siderable role in the biogeochemistry of elements. For example, Geo- reduce extracellular insoluble ferric iron oxides [Fe(III)] to ferrous iron bacter sulfurreducens PCA strain isolated from the surface sediment is [Fe(II)], accompanied by the oxidation of organic matter (e.g., acetate), able to oxidize acetate, coupling with elemental sulfur reduction hydrogen, or ammonium under anaerobic conditions. This microbe- (Caccavo et al., 1994). Phosphorus has a good affinity to Fe(III) oxide mediated process is central to several other biogeochemical cycles in surfaces (Norton et al., 2008) and could be released when Fe(III) mi- various anoxic environments, which, for instance, significantly influ- nerals are reduced by Geobacter genus (Wang et al., 2016). In addition, ence the cycles of carbon (C), nitrogen (N), and phosphorus (P) (Li Geothermobacter, Geoalkalibacter, and Geopsychrobacter also reduce Fe et al., 2012). The most well-known dissimilatory Fe(III) reducers belong (III) oxides, with acetate and amino acids acting as electron donors to in the Geobacteraceae family within the phylum Proteobacteria (Kashefi et al., 2003; Zavarzina et al., 2006; Holmes et al., 2004). (Lovley et al., 2004). This family has thus far been reported to en- Paddy soil is a transitional ecosystem between terrestrial and compass four genera, including Geobacter, Geothermobacter, Geoalk- aquatic ecosystems that is rich in Fe(III) oxides. The redox potential alibacter, and Geopsychrobacter (https://www.arb-silva.de/), with all gradient resulted from frequent alternate cycles of drying and wetting, being involved in dissimilatory Fe(III) reduction (Lovley et al., 2011; as well as an abundance of Fe(III), making paddy soils a potential Tully et al., 2017; Zavarzina et al., 2006; Holmes et al., 2004). These hotspot for dissimilatory iron reduction (Ding et al., 2014). It has been genera are widely distributed in many anaerobic environments, such as previously found that the Geobacter species play a major role in Fe(III) ⁎ Corresponding author at: State Key Lab of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Shuangqing Road, No.18, Haidian District, Beijing 100085, China. E-mail address: [email protected] (L. Ding). https://doi.org/10.1016/j.apsoil.2020.103577 Received 10 September 2019; Received in revised form 23 February 2020; Accepted 2 March 2020 Available online 08 March 2020 0929-1393/ © 2020 Elsevier B.V. All rights reserved. X. Li, et al. Applied Soil Ecology 153 (2020) 103577 reduction coupled to acetate or ammonium oxidation in paddy soils plot in April (early rice) and July (late rice) every year. The rice (Ding et al., 2015; Nercessian et al., 2012; Li et al., 2019). Thus, it seedlings were planted at a spacing of 20 cm × 20 cm (675 plants) per seems reasonable to expect that dissimilatory iron reduction mediated plot. Then, the field was flooded with 3–5 cm height of water for about by the Geobacteraceae family may influence the rice yields by affecting 90 days, and subjected to two-week drainage before harvest at July the biogeochemical cycles of nutrient elements. Therefore, in- (early rice) and October (late rice). During each rice growth period, vestigating the diversity and composition of the Geobacteraceae com- weeding and pest control were performed only once in June (early rice) munities found in paddy soils could provide valuable information for or September (late rice) every year. improving the soil fertility and the productivity of paddy soils. Fertilization is a universal and efficient way to improve rice yields. 2.3. Soil sampling and analyses Chemical and organic fertilization could elevate the soil nutrient levels and may affect the microbial communities found in the soil. For in- In late Aug 2017 (at elongation stage of rice), all plots were sampled stance, Zhong et al. (2010) found that increased levels of total nitrogen independently. At that time point, the field had not been subjected to and available phosphorus under long-term chemical fertilization sig- agronomic interventions such as weeding and pest control for nearly a nificantly influenced the microbial functional diversity in paddy soils month prior to sampling. For each plot five soil cores were collected (Zhong et al., 2010). The continuous input of organic and/or inorganic from the surface layer (0 to 15 cm in depth) by soil auger (diameter fertilizers could affect the overall bacterial community compositions in 5 cm) and completely mixed. Soil samples were then sealed in sterile paddy soils, which is attributed to changes in the levels of organic C, plastic bags and transported to the lab on ice within 24 h. alkali-hydrolyzable nitrogen, and available phosphorus in the soil (Cui Each soil sample was divided into three portions: one was air-dried et al., 2018). The community of dissimilatory iron-reducing bacteria and grounded through a 2-mm sieve for analyses of soil physicochem- was previously found to be significantly altered by long-term nitrogen ical properties in 2 weeks; the second samples were stored at 4 °C for fertilization, possibly due to the alterations in the total C, N, and about 1 month until soil iron speciation analysis; the remaining samples amorphous Fe(III) oxide in paddy soils (Ding et al., 2015). Nevertheless, were stored at −80 °C for about 1 month until molecular analysis. Soil the effects of long-term organic and/or chemical fertilization on the pH was analyzed at a dry soil to ultrapure water ratio of 1:2.5 (w/v) composition and diversity of Geobacteraceae community in paddy soils using a pH meter (FE20; Mettler Toledo, Zurich, Switzerland). Soil total have yet to be fully elucidated. Here, we hypothesize that the Geo- carbon (Total C) and total nitrogen (Total N) were measured using an bacteraceae community shifts due to long-term input of different fer- element analyzer (Vario EL III, Elementar, Germany). Soil organic + tilizers in paddy soils. matter (OM) and ammonium (NH4 -N) were determined by colori- The objectives of the present study were to investigate the changes metric methods of absorbance at 590 nm (A590) and 660 nm (A660), of diversity and composition of Geobacteraceae family in paddy soils respectively (Lu, 1999). Soil dissolved organic C (DOC) and dissolved under long-term chemical and/or organic fertilization practices from total N (DTN) were extracted at a soil to water ratio of 1:5 (w/v) and Southern China, and reveal the main factors influencing the structures determined by a TOC analyzer (LiquicTOC, Elementar, Germany). Soil of Geobacteraceae family in paddy soils. electrical conductivity was determined by a portable conductivity meter (MP521, China). The 2-mm sieved soil sample (0.25 g) was di- 2. Materials and methods gested with aqua regia (3HCl:HNO3, v/v) and condensed by perchloric acid (HClO4). The detailed digestion procedure was described in sup- 2.1. Site description plementary methods. Then the digested soils were analyzed using an inductively coupled plasma optical

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