Abstract
Purpose
Geobacteraceae are important dissimilatory Fe (III)-reducing microorganisms, influencing the cycling of metals, nutrients as well as the degradation of organic contaminants. However, little is known about their distribution, diversity, and abundance of Geobacteraceae and the effects of environment factors and geographic distance on the distribution and diversity of Geobacteraceae in paddy soils remain unclear. Therefore, the objectives of this study were to investigate the distribution, diversity, and abundance of Geobacteraceae in paddy soils and to determine key factors in shaping the Geobacteraceae distribution, environmental factors, geographic distance, or both and to quantify their contribution to Geobacteraceae variation.
Materials and methods
Illumina sequencing and quantitative real-time PCR using a primer set targeting 16S rRNA genes of bacteria affiliated with the family Geobacteraceae were employed to measure the community composition, diversity, and abundance patterns of 16S rRNA genes of Geobacteraceae in 16 samples collected from north to south of China. MRT, Mantel test, and VPA were used to analyze the relationship between communities of Geobacteraceae and environmental factors and geographic distance.
Results and discussion
Quantitative PCR showed that the abundance of 16S rRNA genes of Geobacteraceae ranged from (1.20 ± 0.18) × 108 to 1.13 × 109 ± 2.25 × 108 copies per gram of soil (dry weight) across different types of soils. Illumina sequencing results showed Geobacter was the dominant genus within the family of Geobacteraceae. Multivariate regression tree (MRT) analysis showed that soil amorphous iron contributed more (22.46 %) to the variation of dominant species of Geobacteraceae than other examined soil chemical factors such as pH (14.52 %), ammonium (5.12 %), and dissolved organic carbon (4.74 %). Additionally, more geographically distant sites harbored less similar communities. Variance partitioning analysis (VPA) showed that geographic distance contributed more to the variation of Geobacteraceae than any other factor, although the environmental factors explained more variation when combined. So, we detected the uneven distribution of Geobacteraceae in paddy soils of China and demonstrated that Geobacteraceae community composition was strongly associated with geographic distance and soil chemical factors including aFe, pH, Fe, DOC, C:N, and NO3 −-N. These results greatly expand the knowledge of the distribution of Geobacteraceae in environments, particularly in terrestrial ecosystems.
Conclusions
Our results showed that geographic distance and amorphous iron played important roles in shaping Geobacteraceae community composition and revealed that both geographic distance and soil properties governed Geobacteraceae biogeography in paddy soils. Our findings will be critical in facilitating the prediction of element cycling by incorporating information on functional microbial communities into current biogeochemical models.
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References
Borch T, Kretzschmar R, Kappler A, Cappellen PV, Ginder-Vogel M, Voegelin A, Campbell K (2009) Biogeochemical redox processes and their impact on contaminant dynamics. Environ Sci Technol 44(1):15–23
Burgin AJ, Yang WH, Hamilton SK, Silver WL (2011) Beyond carbon and nitrogen: how the microbial energy economy couples elemental cycles in diverse ecosystems. Front Ecol Environ 9(1):44–52
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6(8):1621–1624
Chao T, Zhou L (1983) Extraction techniques for selective dissolution of amorphous iron oxides from soils and sediments. Soil Sci Soc Am J 47:225–232
Chu H, Fierer N, Lauber CL, Caporaso J, Knight R, Grogan P (2010) Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ Microbiol 12(11):2998–3006
Coates JD, Phillips E, Lonergan DJ, Jenter H, Lovley DR (1996) Isolation of Geobacter species from diverse sedimentary environments. Appl Environ Microbiol (AEM) 62(5):1531–1536
Davison W (1993) Iron and manganese in lakes. Earth-Sci Rev 34(2):119–163
Deng D, Zhang Y, Liu Y (2015) A Geobacter strain isolated from rice paddy soil with higher bioelectricity generation capability in comparison to Geobacter sulfurreducens PCA. RSC Adv 5(55):43978–43989
Ding L-J, Su J-Q, Xu H-J, Jia Z-J, Zhu Y-G (2015) Long-term nitrogen fertilization of paddy soil shifts iron-reducing microbial community revealed by RNA-13C-acetate probing coupled with pyrosequencing. ISME J 9(3):721–734
Feng Y, Grogan P, Caporaso JG, Zhang H, Lin X, Knight R, Chu H (2014) pH is a good predictor of the distribution of anoxygenic purple phototrophic bacteria in Arctic soils. Soil Biol Biochem 74:193–200
Ge Y, He J-z, Zhu Y-g, Zhang J-b, Xu Z, Zhang L-m, Zheng Y-m (2008) Differences in soil bacterial diversity: driven by contemporary disturbances or historical contingencies? ISME J 2(3):254–264
Ge Y, Schimel JP, Holden PA (2012) Identification of soil bacteria susceptible to TiO2 and ZnO nanoparticles. Appl Environ Microbiol 78(18):6749–6758
Griffiths RI, Thomson BC, James P, Bell T, Bailey M, Whiteley AS (2011) The bacterial biogeography of British soils. Environ Microbiol 13(6):1642–1654
Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JB (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10(7):497–506
Holmes DE, Finneran KT, O’neil RA, Lovley DR (2002) Enrichment of members of the family Geobacteraceae associated with stimulation of dissimilatory metal reduction in uranium-contaminated aquifer sediments. Appl Environ Microbiol (AEM) 68(5):2300–2306
Hori T, Müller A, Igarashi Y, Conrad R, Friedrich MW (2010) Identification of iron-reducing microorganisms in anoxic rice paddy soil by 13C-acetate probing. ISME J 4(2):267–278
Hori T, Aoyagi T, Itoh H, Narihiro T, Oikawa A, Suzuki K, Ogata A, Friedrich MW, Conrad R, Kamagata Y (2015) Isolation of microorganisms involved in reduction of crystalline iron (III) oxides in natural environments. Front Microbiol 6:386
Jäckel U, Russo S, Schnell S (2005) Enhanced iron reduction by iron supplement: a strategy to reduce methane emission from paddies. Soil Biol Biochem 37(11):2150–2154
Jiang Y, Liang Y, Li C, Wang F, Sui Y, Suvannang N, Zhou J, Sun B (2016) Crop rotations alter bacterial and fungal diversity in paddy soils across East Asia. Soil Biol Biochem 95:250–261
Kato S, Nakamura R, Kai F, Watanabe K, Hashimoto K (2010) Respiratory interactions of soil bacteria with (semi) conductive iron-oxide minerals. Environ Microbiol 12:3114–3123
Lalonde K, Mucci A, Ouellet A, Gélinas Y (2012) Preservation of organic matter in sediments promoted by iron. Nature 483(7388):198–200
Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75(15):5111–5120
Li H, Peng J, Weber KA, Zhu Y (2011) Phylogenetic diversity of Fe (III)-reducing microorganisms in rice paddy soil: enrichment cultures with different short-chain fatty acids as electron donors. J Soils Sediments 11(7):1234–1242
Liu J, Sui Y, Yu Z, Shi Y, Chu H, Jin J, Liu X, Wang G (2014) High throughput sequencing analysis of biogeographical distribution of bacterial communities in the black soils of northeast China. Soil Biol Biochem 70:113–122
Liu J, Sui Y, Yu Z, Shi Y, Chu H, Jin J, Liu X, Wang G (2015) Soil carbon content drives the biogeographical distribution of fungal communities in the black soil zone of northeast China. Soil Biol Biochem 83:29–39
Lovley DR (1987) Organic matter mineralization with the reduction of ferric iron: a review. Geomicrobiol J 5(3–4):375–399
Lovley DR, Holmes DE, Nevin KP (2004) Dissimilatory Fe (iii) and Mn (iv) reduction. Adv Microb Physiol 49:219–286
Mejia J, Roden EE, Ginder-Vogel MA (2016) Influence of oxygen and nitrate on Fe (hydr) oxide mineral transformation and soil microbial communities during redox cycling. Environ Sci Technol 50:3580–3588
Melton ED, Swanner ED, Behrens S, Schmidt C, Kappler A (2014) The interplay of microbially mediated and abiotic reactions in the biogeochemical Fe cycle. Nat Rev Microbiol 12(12):797–808
Pierra M, Carmona-Martínez AA, Trably E, Godon J-J, Bernet N (2015) Microbial characterization of anode-respiring bacteria within biofilms developed from cultures previously enriched in dissimilatory metal-reducing bacteria. Bioresour Technol 195:283–287
Reed DC, Algar CK, Huber JA, Dick GJ (2014) Gene-centric approach to integrating environmental genomics and biogeochemical models. Proc Natl Acad Sci U S A 111(5):1879–1884
Rodrigues JL, Pellizari VH, Mueller R, Baek K, Jesus EC, Paula FS, Mirza B, Hamaoui GS, Tsai SM, Feigl B (2013) Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. Proc Natl Acad Sci U S A 110(3):988–993
Snoeyenbos-West O, Nevin K, Anderson R, Lovley D (2000) Enrichment of Geobacter species in response to stimulation of Fe (III) reduction in sandy aquifer sediments. Microb Ecol 39(2):153–167
Stumm W, Sulzberger B (1992) The cycling of iron in natural environments: considerations based on laboratory studies of heterogeneous redox processes. Geochim Cosmochim Acta 56(8):3233–3257
Wang N, Chen Z, Li H-B, Su J-Q, Zhao F, Zhu Y-G (2015) Bacterial community composition at anodes of microbial fuel cells for paddy soils: the effects of soil properties. J Soils Sediments 15(4):926–936
Weber KA, Achenbach LA, Coates JD (2006) Microbes pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol 4:752–764
Yi W, You J, Zhu C, Wang B, Qu D (2013) Diversity, dynamic and abundance of Geobacteraceae species in paddy soil following slurry incubation. Eur J Soil Biol 56:11–18
Zhang S, Zhao F, Sun G, Su J, Yang X, Li H, Zhu Y (2015) Diversity and Abundance of Arsenic Biotransformation Genes in Paddy Soils from Southern China. Environ Sci Technol 49: 4138–4146
Acknowledgments
This work was supported by the National Natural Science Foundation of China (41430858) and the Strategic Priority Research Program of Chinese Academy of Sciences (XDB15020402).
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Yuan, HY., Ding, LJ., Wang, N. et al. Geographic distance and amorphous iron affect the abundance and distribution of Geobacteraceae in paddy soils in China. J Soils Sediments 16, 2657–2665 (2016). https://doi.org/10.1007/s11368-016-1462-x
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DOI: https://doi.org/10.1007/s11368-016-1462-x