Lignocellulosic fraction-induced niche differentiation within dissimilatory iron reducing bacterial groups in a paddy soil

Abstract

● Responses of soil DIRB to lignocellulosic fractions during a 6-week microcosm incubation were investigated.

● Anaeromyxobacter , Bacillus , and Clostridium maintained their dominance throughout the incubation.

● Distinct DIRB groups proliferated under specific lignocellulosic fraction amendments.

● Limits of insufficient ferric iron on the proliferation varied by DIRB group.

Dissimilatory iron reducing bacteria (DIRB) are phylogenetically and physiologically diverse in paddy soils, where iron reduction closely couples with the oxidation of rice straw-derived carbon in the straw returning scenarios. However, few studies have addressed the niche differentiation within DIRB groups during the degradation of lignocellulosic fractions of rice straw. This study conducted a 6-week microcosm incubation experiment to reveal the distinct responses of DIRB groups under specific lignocellulosic fraction amendments with and without ferrihydrite (Fh) addition in a flooded paddy Ultisol. Results showed that the total absolute abundance of the 19 detected DIRB groups did not vary significantly during the incubation. Anaeromyxobacter, Bacillus, and Clostridium were the dominant DIRB groups for all lignocellulosic treatments whereas Thermincola was dominant but only under xylan amendment with Fh addition. DIRB-nodes in the co-occurrence networks of bacterial community mainly belonged to Anaeromyxobacter and Bacillus. Clostridium and Thermincola, Alkaliphilus and Anaeromyxobacter, and Alicyclobacillus, Desulfobulbus, and Desulfosporosinus were specifically proliferated under xylan, cellulose, and lignin amendments, respectively. Whether the proliferation was limited by insufficient ferric iron varied by bacterial group. These findings suggested the lignocellulosic fraction-induced niche differentiation within DIRB groups, which advanced our understanding of the ecology of DIRB in paddy soils under straw returning.

Graphical abstract

Keywords

cellulose / hemicellulose / lignin / bacterial community diversity / co-occurrence networks

References

[1] Asina, F.N.U., Brzonova, I., Kozliak, E., Kubátová, A., Ji, Y., 2017. Microbial treatment of industrial lignin: Successes, problems and challenges. Renewable & Sustainable Energy Reviews77, 1179–1205.

[2] Bao, Y., Dolfing, J., Wang, B., Chen, R., Huang, M., Li, Z., Lin, X., Feng, Y., 2019. Bacterial communities involved directly or indirectly in the anaerobic degradation of cellulose. Biology and Fertility of Soils55, 201–211.

[3] Bastian, F., Bouziri, L., Nicolardot, B., Ranjard, L., 2009. Impact of wheat straw decomposition on successional patterns of soil microbial community structure. Soil Biology & Biochemistry41, 262–275.

[4] Benjamini, Y., Hochberg, Y., 1995. Controling the false discovery rate—a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B Methodological57, 289–300.

[5] Bolyen, E., Rideout, J.R., Dillon, M.R., Bokulich, N.A., Abnet, C.C., Al-Ghalith, G.A., Alexander, H., Alm, E.J., Arumugam, M., Asnicar, F., Bai, Y., Bisanz, J.E., Bittinger, K., Brejnrod, A., Brislawn, C.J., Brown, C.T., Callahan, B.J., Caraballo-Rodríguez, A.M., Chase, J., Cope, E.K., Da Silva, R., Diener, C., Dorrestein, P.C., Douglas, G.M., Durall, D.M., Duvallet, C., Edwardson, C.F., Ernst, M., Estaki, M., Fouquier, J., Gauglitz, J.M., Gibbons, S.M., Gibson, D.L., Gonzalez, A., Gorlick, K., Guo, J., Hillmann, B., Holmes, S., Holste, H., Huttenhower, C., Huttley, G.A., Janssen, S., Jarmusch, A.K., Jiang, L., Kaehler, B.D., Kang, K.B., Keefe, C.R., Keim, P., Kelley, S.T., Knights, D., Koester, I., Kosciolek, T., Kreps, J., Langille, M.G.I., Lee, J., Ley, R., Liu, Y.X., Loftfield, E., Lozupone, C., Maher, M., Marotz, C., Martin, B.D., McDonald, D., McIver, L.J., Melnik, A.V., Metcalf, J.L., Morgan, S.C., Morton, J.T., Naimey, A.T., Navas-Molina, J.A., Nothias, L.F., Orchanian, S.B., Pearson, T., Peoples, S.L., Petras, D., Preuss, M.L., Pruesse, E., Rasmussen, L.B., Rivers, A., Robeson, M.S. II, Rosenthal, P., Segata, N., Shaffer, M., Shiffer, A., Sinha, R., Song, S.J., Spear, J.R., Swafford, A.D., Thompson, L.R., Torres, P.J., Trinh, P., Tripathi, A., Turnbaugh, P.J., Ul-Hasan, S., van der Hooft, J.J.J., Vargas, F., Vázquez-Baeza, Y., Vogtmann, E., von Hippel, M., Walters, W., Wan, Y., Wang, M., Warren, J., Weber, K.C., Williamson, C.H.D., Willis, A.D., Xu, Z.Z., Zaneveld, J.R., Zhang, Y., Zhu, Q., Knight, R., Caporaso, J.G., 2019. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology37, 852–857.

[6] Caccavo, F. Jr, Lonergan, D.J., Lovley, D.R., Davis, M., Stolz, J.F., McInerney, M.J., 1994. Geobacter sulfurreducens sp. nov., a hydrogen-and acetate-oxidizing dissimilatory metal-reducing microorganism. Applied and Environmental Microbiology60, 3752–3759.

[7] Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A., Holmes, S.P., 2016. DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods13, 581–583.

[8] Chen, M., Jiang, H.L., 2016. Relative contribution of iron reduction to sediments organic matter mineralization in contrasting habitats of a shallow eutrophic freshwater lake. Environmental Pollution213, 904–912.

[9] Chen, S., Zhou, Y., Chen, Y., Gu, J., 2018. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics (Oxford, England)34, i884–i890.

[10] Cragg, S.M., Beckham, G.T., Bruce, N.C., Bugg, T.D., Distel, D.L., Dupree, P., Etxabe, A.G., Goodell, B.S., Jellison, J., McGeehan, J.E., McQueen-Mason, S.J., Schnorr, K., Walton, P.H., Watts, J.E.M., Zimmer, M., 2015. Lignocellulose degradation mechanisms across the Tree of Life. Current Opinion in Chemical Biology29, 108–119.

[11] Deng, Y., Jiang, Y.H., Yang, Y., He, Z., Luo, F., Zhou, J., 2012. Molecular ecological network analyses. BMC Bioinformatics13, 113.

[12] Ding, B., Zhang, H., Luo, W., Sun, S., Cheng, F., Li, Z., 2021. Nitrogen loss through denitrification, anammox and Feammox in a paddy soil. Science of the Total Environment773, 145601.

[13] Ding, L.J., Li, X.M., Wang, Y.F., Luo, C.Y., Wang, X.D., Duan, G.L., Zhu, Y.G., 2022. Influences of arsenate and/or phosphate adsorption to ferrihydrite on iron-reducing and arsenic-reducing microbial communities in paddy soil revealed by rRNA-¹³C-acetate probing. Soil Biology & Biochemistry169, 108679.

[14] 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 Journal9, 721–734.

[15] Duan, X., Li, Z., Li, Y., Yuan, H., Gao, W., Chen, X., Ge, T., Wu, J., Zhu, Z., 2023. Iron–organic carbon associations stimulate carbon accumulation in paddy soils by decreasing soil organic carbon priming. Soil Biology & Biochemistry179, 108972.

[16] Fang, Y., Singh, B.P., Collins, D., Armstrong, R., Van Zwieten, L., Tavakkoli, E., 2020. Nutrient stoichiometry and labile carbon content of organic amendments control microbial biomass and carbon-use efficiency in a poorly structured sodic-subsoil. Biology and Fertility of Soils56, 219–233.

[17] Gan, C., Wu, R., Luo, Y., Song, J., Luo, D., Li, B., Yang, Y., Xu, M., 2021. Visualizing and isolating iron-reducing microorganisms at the single-cell level. Applied and Environmental Microbiology87, e02192-20.

[18] Goberna, M., Verdú, M., 2022. Cautionary notes on the use of co-occurrence networks in soil ecology. Soil Biology & Biochemistry166, 108534.

[19] Guimera, R., Amaral, L.A.N., 2005. Functional cartography of complex metabolic networks. Nature433, 895–900.

[20] Guo, T., Zhang, Q., Ai, C., Liang, G., He, P., Lei, Q., Zhou, W., 2020. Analysis of microbial utilization of rice straw in paddy soil using a DNA‐SIP approach. Soil Science Society of America Journal84, 99–114.

[21] Hansel, C.M., Benner, S.G., Nico, P., Fendorf, S., 2004. Structural constraints of ferric (hydr)oxides on dissimilatory iron reduction and the fate of Fe(II). Geochimica et Cosmochimica Acta68, 3217–3229.

[22] Hori, T., Aoyagi, T., Itoh, H., Narihiro, T., Oikawa, A., Suzuki, K., Ogata, A., Friedrich, M.W., Conrad, R., Kamagata, Y., 2015. Isolation of microorganisms involved in reduction of crystalline iron(III) oxides in natural environments. Frontiers in Microbiology6, 386.

[23] Ji, Y., Liu, P., Conrad, R., 2018. Response of fermenting bacterial and methanogenic archaeal communities in paddy soil to progressing rice straw degradation. Soil Biology & Biochemistry124, 70–80.

[24] Kögel-Knabner, I., 2017. The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter: fourteen years on. Soil Biology & Biochemistry105, A3–A8.

[25] Kwon, M.J., O’Loughlin, E.J., Boyanov, M.I., Brulc, J.M., Johnston, E.R., Kemner, K.M., Antonopoulos, D.A., 2016. Impact of organic carbon electron donors on microbial community development under iron-and sulfate-reducing conditions. PLoS One11, e0146689.

[26] Lentini, C.J., Wankel, S.D., Hansel, C.M., 2012. Enriched iron (III)-reducing bacterial communities are shaped by carbon substrate and iron oxide mineralogy. Frontiers in Microbiology3, 404.

[27] Levy-Booth, D.J., Navas, L.E., Fetherolf, M.M., Liu, L.Y., Dalhuisen, T., Renneckar, S., Eltis, L.D., Mohn, W.W., 2022. Discovery of lignin-transforming bacteria and enzymes in thermophilic environments using stable isotope probing. ISME Journal16, 1944–1956.

[28] Li, H., Dai, M., Dai, S., Dong, X., 2018. Current status and environment impact of direct straw return in China’s cropland–A review. Ecotoxicology and Environmental Safety159, 293–300.

[29] Li, H., Peng, J., Weber, K.A., 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. Journal of Soils and Sediments11, 1234–1242.

[30] Li, H.J., Peng, J.J., Li, H.B., 2012. Diversity and characterization of potential H₂-dependent Fe(III)-reducing bacteria in paddy soils. Pedosphere22, 673–680.

[31] Liu, H., Wang, H., 2016. Characterization of Fe(III)-reducing enrichment culture and isolation of Fe(III)-reducing bacterium Enterobacter sp. L6 from marine sediment. Journal of Bioscience and Bioengineering 122, 92–96

[32] Liu, X., Bayard, R., Benbelkacem, H., Buffière, P., Gourdon, R., 2015. Evaluation of the correlations between biodegradability of lignocellulosic feedstocks in anaerobic digestion process and their biochemical characteristics. Biomass and Bioenergy81, 534–543.

[33] Luo, D., Yu, H., Li, Y., Yu, Y., Chapman, S.J., Yao, H., 2023. A joint role of iron oxide and temperature for methane production and methanogenic community in paddy soils. Geoderma433, 116462.

[34] Magoč, T., Salzberg, S.L., 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics (Oxford, England)27, 2957–2963.

[35] Maslov, S., Sneppen, K., 2002. Specificity and stability in topology of protein networks. Science296, 910–913.

[36] Newsome, L., Lopez Adams, R., Downie, H.F., Moore, K.L., Lloyd, J.R., 2018. NanoSIMS imaging of extracellular electron transport processes during microbial iron(III) reduction. FEMS Microbiology Ecology94, fiy104.

[37] Nixon, S.L., Telling, J.P., Wadham, J.L., Cockell, C.S., 2017. Viable cold-tolerant iron-reducing microorganisms in geographically diverse subglacial environments. Biogeosciences14, 1445–1455.

[38] Olesen, J., Bascompte, J., Dupont, Y., Jordano, P., 2007. The modularity of pollination networks. Proceedings of the National Academy of Sciences of the United States of America104, 19891–19896.

[39] Pankratova, G., Hederstedt, L., Gorton, L., 2019. Extracellular electron transfer features of Gram-positive bacteria. Analytica Chimica Acta1076, 32–47.

[40] Peng, Q.A., Shaaban, M., Wu, Y., Hu, R., Wang, B., Wang, J., 2016. The diversity of iron reducing bacteria communities in subtropical paddy soils of China. Applied Soil Ecology101, 20–27.

[41] Pérez-Rodríguez, I., Rawls, M., Coykendall, D.K., Foustoukos, D.I., 2016. Deferrisoma palaeochoriense sp. nov., a thermophilic, iron(III)-reducing bacterium from a shallow-water hydrothermal vent in the Mediterranean Sea. International Journal of Systematic and Evolutionary Microbiology66, 830–836.

[42] Persinoti, G.F., Paixão, D.A., Bugg, T.D., Squina, F.M., 2018. Genome sequence of Lysinibacillus sphaericus, a lignin-degrading bacterium isolated from municipal solid waste soil. Genome Announcements6, e00353-18.

[43] Pester, M., Bittner, N., Deevong, P., Wagner, M., Loy, A., 2010. A ‘rare biosphere’ microorganism contributes to sulfate reduction in a peatland. ISME Journal4, 1591–1602.

[44] Porsch, K., Meier, J., Kleinsteuber, S., Wendt-Potthoff, K., 2009. Importance of different physiological groups of iron reducing microorganisms in an acidic mining lake remediation experiment. Microbial Ecology57, 701–717.

[45] Rosnow, J.J., Anderson, L.N., Nair, R.N., Baker, E.S., Wright, A.T., 2017. Profiling microbial lignocellulose degradation and utilization by emergent omics technologies. Critical Reviews in Biotechnology37, 626–640.

[46] Schwertmann, U., Cornell, R.M., 2000. Iron Oxides in the Laboratory: Preparation and Characterization (2nd ed.). Wiley-VCH Verlag GmbH & Co. Weinheim, Germany

[47] Shi, L., Dong, H., Reguera, G., Beyenal, H., Lu, A., Liu, J., Yu, H.Q., Fredrickson, J.K., 2016. Extracellular electron transfer mechanisms between microorganisms and minerals. Nature Reviews Microbiology14, 651–662.

[48] Shinde, R., Shahi, D.K., Mahapatra, P., Naik, S.K., Thombare, N., Singh, A.K., 2022. Potential of lignocellulose degrading microorganisms for agricultural residue decomposition in soil: A review. Journal of Environmental Management320, 115843.

[49] Su, C., Zhang, M., Lin, L., Yu, G., Zhong, H., Chong, Y., 2020. Reduction of iron oxides and microbial community composition in iron-rich soils with different organic carbon as electron donors. International Biodeterioration & Biodegradation148, 104881.

[50] Viollier, E., Inglett, P.W., Hunter, K., Roychoudhury, A.N., Van Cappellen, P., 2000. The ferrozine method revisited: Fe(II)/Fe(III) determination in natural waters. Applied Geochemistry15, 785–790.

[51] Wang, C., Thielemann, L., Dippold, M.A., Guggenberger, G., Kuzyakov, Y., Banfield, C.C., Ge, T., Guenther, S., Bork, P., Horn, M.A., Dorodnikov, M., 2022. Microbial iron reduction compensates for phosphorus limitation in paddy soils. Science of the Total Environment837, 155810.

[52] Wang, J., Deng, H., Wu, S.S., Deng, Y.C., Liu, L., Han, C., Jiang, Y.B., Zhong, W.H., 2019. Assessment of abundance and diversity of exoelectrogenic bacteria in soil under different land use types. Catena172, 572–580.

[53] Wang, K., Jia, R., Li, L., Jiang, R., Qu, D., 2020. Community structure of Anaeromyxobacter in Fe(III) reducing enriched cultures of paddy soils. Journal of Soils and Sediments20, 1621–1631.

[54] Wang, W., Lai, D.Y.F., Wang, C., Pan, T., Zeng, C., 2015. Effects of rice straw incorporation on active soil organic carbon pools in a subtropical paddy field. Soil & Tillage Research152, 8–16.

[55] Wang, X.J., Yang, J., Chen, X.P., Sun, G.X., Zhu, Y.G., 2009. Phylogenetic diversity of dissimilatory ferric iron reducers in paddy soil of Hunan, South China. Journal of Soils and Sediments9, 568–577.

[56] Wang, Y., Wu, P., Mei, F., Ling, Y., Qiao, Y., Liu, C., Leghari, S.J., Guan, X., Wang, T., 2021. Does continuous straw returning keep China farmland soil organic carbon continued increase? A Meta-analysis.. Journal of Environmental Management288, 112391.

[57] Weber, K.A., Achenbach, L.A., Coates, J.D., 2006. Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nature Reviews Microbiology4, 752–764.

[58] Wegner, C.E., Liesack, W., 2016. Microbial community dynamics during the early stages of plant polymer breakdown in paddy soil. Environmental Microbiology18, 2825–2842.

[59] Wei, X., Zhu, Z., Wei, L., Wu, J., Ge, T., 2019. Biogeochemical cycles of key elements in the paddy-rice rhizosphere: microbial mechanisms and coupling processes. Rhizosphere10, 100145.

[60] Xiao, B., Sun, X., Sun, R., 2001. Chemical, structural, and thermal characterizations of alkali-soluble lignins and hemicelluloses, and cellulose from maize stems, rye straw, and rice straw. Polymer Degradation & Stability74, 307–319.

[61] Xu, J.X., Li, X.M., Sun, G.X., Cui, L., Ding, L.J., He, C., Li, L.G., Shi, Q., Smets, B.F., Zhu, Y.G., 2019. Fate of labile organic carbon in paddy soil is regulated by microbial ferric iron reduction. Environmental Science & Technology53, 8533–8542.

[62] Xu, Y., He, Y., Feng, X., Liang, L., Xu, J., Brookes, P.C., Wu, J., 2014. Enhanced abiotic and biotic contributions to dechlorination of pentachlorophenol during Fe (III) reduction by an iron-reducing bacterium Clostridium beijerinckii Z. Science of the Total Environment473, 215–223.

[63] Yu, H.Y., Li, F.B., Liu, C.S., Huang, W., Liu, T.X., Yu, W.M., 2016. Iron redox cycling coupled to transformation and immobilization of heavy metals: implications for paddy rice safety in the red soil of South China. Advances in Agronomy137, 279–317.

[64] Yuan, H.Y., Ding, L.J., Wang, N., Chen, S.C., Deng, Y., Li, X.M., Zhu, Y.G., 2016. Geographic distance and amorphous iron affect the abundance and distribution of Geobacteraceae in paddy soils in China. Journal of Soils and Sediments16, 2657–2665.

[65] Zavarzina, D.G., Sokolova, T.G., Tourova, T.P., Chernyh, N.A., Kostrikina, N.A., Bonch-Osmolovskaya, E.A., 2007. Thermincola ferriacetica sp. nov., a new anaerobic, thermophilic, facultatively chemolithoautotrophic bacterium capable of dissimilatory Fe(III) reduction. Extremophiles11, 1–7.

[66] Zhang, Z., Qu, Y., Li, S., Feng, K., Wang, S., Cai, W., Liang, Y., Li, H., Xu, M., Yin, H., Deng, Y., 2017. Soil bacterial quantification approaches coupling with relative abundances reflecting the changes of taxa. Scientific Reports7, 4837.

[67] Zhilina, T.N., Zavarzina, D.G., Kolganova, T.V., Lysenko, A.M., Tourova, T.P., 2009. Alkaliphilus peptidofermentans sp. nov., a new alkaliphilic bacterial soda lake isolate capable of peptide fermentation and Fe(III) reduction. Microbiology78, 445–454.

[68] Zhou, J.Z., Deng, Y., Luo, F., He, Z.L., Tu, Q.C., Zhi, X.Y., 2010. Functional molecular ecological networks. mBio1, e00169-10.

[69] Zhuang, Y., Zhu, J., Shi, L., Fu, Q., Hu, H., Huang, Q., 2022. Influence mechanisms of iron, aluminum and manganese oxides on the mineralization of organic matter in paddy soil. Journal of Environmental Management301, 113916.

RIGHTS & PERMISSIONS

Higher Education Press