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Composition and key-influencing factors of bacterial communities active in sulfur cycling of soda lake sediments

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Abstract

Bacteria are important participants in sulfur cycle of the extremely haloalkaline environment, e.g. soda lake. The effects of physicochemical factors on the composition of sulfide-oxidizing bacteria (SOB) and sulfate-reducing bacteria (SRB) in soda lake have remained elusive. Here, we surveyed the community structure of total bacteria, SOB and SRB based on 16S rRNA, soxB and dsrB gene sequencing, respectively, in five soda lakes with different physicochemical factors. The results showed that the dominant bacteria belonged to the phyla Proteobacteria, Bacteroidetes, Halanaerobiaeota, Firmicutes and Actinobacteria. SOB and SRB were widely distributed in lakes with different physicochemical characteristics, and the community composition were different. In general, salinity and inorganic nitrogen sources (NH4+-N, NO3−-N) were the most significant factors. Specifically, the communities of SOB, mainly including Thioalkalivibrio, Burkholderia, Paracoccus, Bradyrhizobium, and Hydrogenophaga genera, were remarkably influenced by the levels of NH4+-N and salinity. Yet, for SRB communities, including Desulfurivibrio, Candidatus Electrothrix, Desulfonatronospira, Desulfonatronum, Desulfonatronovibrio, Desulfonatronobacter and so on, the most significant determinants were salinity and NO3−-N. Besides, Rhodoplanes played a significant role in the interaction between SOB and SRB. From our results, the knowledge regarding the community structures of SOB and SRB in extremely haloalkaline environment was extended.

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References

  • Asnicar F, Weingart G, Tickle TL, Huttenhower C, Segata N (2015) Compact graphical representation of phylogenetic data and metadata with GraPhlAn. PeerJ 3:e1029

    PubMed  PubMed Central  Google Scholar 

  • Banerjee S, Schlaeppi K, van der Heijden MG (2018) Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microb 16(9):567–576

    CAS  Google Scholar 

  • Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. Icwsm 8:361–362

    Google Scholar 

  • Berben T, Overmars L, Sorokin DY, Muyzer G (2019) Diversity and distribution of sulfur oxidation-related genes in Thioalkalivibrio, a genus of chemolithoautotrophic and haloalkaliphilic sulfur-oxidizing bacteria. Front Microbio. https://doi.org/10.3389/fmicb.2019.00160

    Article  Google Scholar 

  • Bjerg JT, Boschker HT, Larsen S, Berry D, Schmid M, Millo D, Tataru P, Meysman FJR, Wagner M, Nielsen LP, Schramm A (2018) Long-distance electron transport in individual, living cable bacteria. Proc Natl Acad Sci 115(22):5786–5791

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bokulich NA, Kaehler BD, Ram RJ, Matthew D, Evan B, Rob K, Huttley GA, Gregory CJ (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with qiime 2’s q2-feature-classifier plugin. Microbiome 6(1):90

    PubMed  PubMed Central  Google Scholar 

  • Chakravarthy SK, Ramaprasad EVV, Shobha E, Sasikala C, Ramana CV (2012) Rhodoplanes piscinae sp. nov isolated from pond water. Int J Syst Evol Microb 62(12):2828–2834

    Google Scholar 

  • Chidthaisong A, Conrad R (2000) Turnover of glucose and acetate coupled to reduction of nitrate, ferric iron and sulfate and to methanogenesis in anoxic rice field soil. FEMS Microb Ecol 31(1):73–86

    CAS  Google Scholar 

  • Edwardson CF, Hollibaugh JT (2018) Composition and activity of microbial communities along the redox gradient of an alkaline, hypersaline, lake. Front Microb. https://doi.org/10.3389/fmicb.2018.00014

    Article  Google Scholar 

  • Foti M, Ma S, Sorokin DY, Rademaker JLW, Kuenen JG, Muyzer G (2006) Genetic diversity and biogeography of haloalkaliphilic sulphur-oxidizing bacteria belonging to the genus Thioalkalivibrio. FEMS Microb Ecol 56(1):95–101

    CAS  Google Scholar 

  • Furian S, Martins ERC, Parizotto TM, Rezende-Filho AT, Victoria RL, Barbiero L (2013) Chemical diversity and spatial variability in myriad lakes in Nhecolandia in the Pantanal wetlands of Brazil. Limnol Oceanogr 58(6):2249–2261

    CAS  Google Scholar 

  • Gao P, Tian H, Li G, Sun HW, Ma T (2015) Microbial diversity and abundance in the Xinjiang Luliang long-term water-flooding petroleum reservoir. Microbiologyopen 4(2):332–342

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ghosh W, Dam B (2009) Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea. FEMS Microb Rev 33(6):999–1043

    CAS  Google Scholar 

  • Giloteaux L, Duran R, Casiot C, Bruneel O, Elbaz-Poulichet F, Goñi-Urriza M (2013) Three-year survey of sulfate-reducing bacteria community structure in Carnoules acid mine drainage (France), highly contaminated by arsenic. FEMS Microb Ecol 83(3):724–737

    CAS  Google Scholar 

  • Gorlenko VM (2007) Anoxygenic phototrophic bacteria from soda lakes. Trans Winogradsky Inst Microb 14:159–183

    Google Scholar 

  • Grant WD, Sorokin DY (2011) Distribution and diversity of soda lake Alkaliphiles. Extremophiles Handbook 1:27–54

    Google Scholar 

  • Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5(3):299–314

    Google Scholar 

  • Jung MY, Pham VH, Park SJ, Kim SJ, Chae JC, Roh Y, Rhee SK (2010) Metagenomic assessment of a sulfur-oxidizing enrichment culture derived from marine sediment. J Microb 48(6):739–747

    CAS  Google Scholar 

  • Katoh K, Misawa K, Kuma KI, Miyata T (2002) Mafft: a novel method for rapid multiple sequence alignment based on fast fourier transform. Nucleic Acids Res 30(14):3059–3066

    CAS  PubMed  PubMed Central  Google Scholar 

  • Koljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martín MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Scott JA, Senés C, Smith ME, Suija A, Taylor DL, Telleria MT, Weiss M, Larsson KH (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22(21):5271–5277

    CAS  PubMed  Google Scholar 

  • Liu ZX, Yang MH, Mu TZ, Liu JL, Xing JM (2021) Transcriptional response of Thialkalivibrio versutus D301 to different sulfur sources and identification of the sulfur oxidation pathways. J Biotechnol 329:160–169

    CAS  PubMed  Google Scholar 

  • Martin M (2011) Cut adapt removes adapter sequences from high-throughput sequencing reads. EMB Net 17(1):10–12

    Google Scholar 

  • Melton ED, Sorokin DY, Overmars L, Chertkov O, Clum A, Pillay M, Ivanova N, Shapiro N, Kyrpides NC, Woyke T (2016) Complete genome sequence of Desulfurivibrio alkaliphilus strain AHT2T, a haloalkaliphilic sulfidogen from Egyptian hypersaline alkaline lakes. Stand Genom Sci 11:67

    Google Scholar 

  • Meyer B, Imhoff JF, Kuever J (2007) Molecular analysis of the distribution and phylogeny of the soxB gene among sulfur-oxidizing bacteria-evolution of the sox sulfur oxidation enzyme system. Env Microb 9(12):2957–2977

    CAS  Google Scholar 

  • Mu TZ, Zhou JM, Yang MH, Xing JM (2016) Complete genome sequence of Thialkalivibrio versutus D301 isolated from soda lake in northern China, a typical strain with great ability to oxidize sulfide. J Biotechnol 227:21–22

    CAS  PubMed  Google Scholar 

  • Müller H, Marozava S, Probs AJ, Meckenstock RU (2020) Groundwater cable bacteria conserve energy by sulfur disproportionation. ISME J 14(2):623–634

    PubMed  Google Scholar 

  • Ni GF, Harnawan P, Seidel L, Heijne AT, Sleutels T, Buisman CJN, Dopson M (2019) Haloalkaliphilic microorganisms assist sulfide removal in a microbial electrolysis cell. J Hazard Mater 363:197–204

    CAS  PubMed  Google Scholar 

  • Nielsen LP, Risgaard-Petersen N, Fossing H, Christensen PB, Sayama M (2010) Electric currents couple spatially separated biogeochemical processes in marine sediment. Nature 463(7284):1071–1074

    CAS  PubMed  Google Scholar 

  • Okamura K, Kanbe T, Hiraishi A (2009) Rhodoplanes serenus sp. nov, a purple non-sulfur bacterium isolated from pond water. Int J Syst Evol Microb 59(3):531–535

    CAS  Google Scholar 

  • Poser A, Lohmayer R, Vogt C, Knoeller K, Kai F (2013) Disproportionation of elemental sulfur by haloalkaliphilic bacteria from soda lakes. Extremophiles 17:1003–1012

    CAS  PubMed  Google Scholar 

  • Price MN, Dehal PS, Arkin AP (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26(7):1641–1650

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rastogi G, Stetler LD, Peyton BM, Sani RK (2009) Molecular analysis of prokaryotic diversity in the deep subsurface of the former homestake gold mine, South Dakota, USA. J Microb 47(4):371–384

    Google Scholar 

  • Rojas P, Rodríguez N, Fuente V, Sánchez-Mata D, Amils R, Sanz JL (2018) Microbial diversity associated with the anaerobic sediments of a soda lake (Mono Lake, California, USA). Can J Microb 64:385–392

    CAS  Google Scholar 

  • Santisteban JI, Mediavilla R, López-Pamo E, Dabrio CJ, Blanca Ruiz Zapata M, José Gil García M, Castaño S, Martínez-Alfaro PE (2004) Loss on ignition: a qualitative or quantitative method for organic matter and carbonate mineral content in sediments? J Paleolimnol 32(3):287–299

    Google Scholar 

  • Schagerl M, Renaut RW (2016) Dipping into the soda lakes of East Africa. In: Schagerl M (ed) Soda lakes of East Africa. Springer, Switzerland, pp 3–24

    Google Scholar 

  • Sharshar MM, Samak NA, Ambreen S, Hao XM, Mu TZ, Maarouf M, Zheng C, Gao YB, Liu ZX, Jia YP, Li XY, Zhong W, Peh S, Yang MH, Xing JM (2020) Improving confirmed nanometric sulfur bioproduction using engineered Thioalkalivibrio versutus. Bioresour Technol 317:124018

    CAS  PubMed  Google Scholar 

  • Sheibley RW, Duff JH, Jackman AP, Triska FJ (2003) Inorganic nitrogen transformations in the bed of the Shingobee River, Minnesota: Integrating hydrologic and biological processes using sediment perfusion cores. Limnol Oceanogr 48(3):1129–1140

    CAS  Google Scholar 

  • Shi Y, Delgado-Baquerizo M, Li Y, Yang YF, Zhu YG, Peñuelas J, Chu HY (2020) Abundance of kinless hubs within soil microbial networks are associated with high functional potential in agricultural ecosystems. Env Int 142:105869

    CAS  Google Scholar 

  • Sorokin DY, Kuenen JG (2005) Haloalkaliphilic sulfur-oxidizing bacteria in soda lakes. FEMS Microb Rev 29:685–702

    CAS  Google Scholar 

  • Sorokin DY, Detkova EN, Muyzer G (2011a) Sulfur-dependent respiration under extremely haloalkaline conditions in soda lake ‘acetogens’ and the description of Natroniella sulfidigena sp. nov. FEMS Microb Lett 319:88–95

    CAS  Google Scholar 

  • Sorokin DY, Kuenen JG, Muyzer G (2011b) The Microbial sulfur cycle at extremely haloalkaline conditions of soda lakes. Front Microb 2:44

    CAS  Google Scholar 

  • Sorokin DY, Banciu HL, Muyzer G (2015) Functional microbiology of soda lakes. Curr Opin Microb 25:88–96

    CAS  Google Scholar 

  • Sorokin DY (2017) Anaerobic haloalkaliphiles. In: eLS. Wiley, Chichester. https://doi.org/10.1002/9780470015902.a0027654

    Chapter  Google Scholar 

  • Tian H, Gao P, Chen Z, Li Y, Li Y, Wang Y, Zhou J, Li G, Ma T (2017) Compositions and abundances of sulfate-reducing and sulfur-oxidizing microorganisms in water-flooded petroleum reservoirs with different temperatures in China. Front Microb 8:143

    Google Scholar 

  • Tourova TP, Slobodova NV, Bumazhkin BK, Kolganova TV, Muyzer G, Sorokin DY (2013) Analysis of community composition of sulfur-oxidizing bacteria in hypersaline and soda lakes using soxB as a functional molecular marker. FEMS Microb Ecol 84(2):280–289

    CAS  Google Scholar 

  • Trojan D, Schreiber L, Bjerg JT, Bøggild A, Yang TT, Kjeldsen KU, Schramm A (2016) A taxonomic framework for cable bacteria and proposal of the candidate genera Electrothrix and Electronema. Syst Appl Microb 39:297–306

    Google Scholar 

  • White JR, Nagarajan N, Pop M (2009) Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 5(4):e1000352

    PubMed  PubMed Central  Google Scholar 

  • Xu DY, Kang XW, Zhuang DF, Pan JJ (2010) Multi-scale quantitative assessment of the relative roles of climate change and human activities in desertification-A case study of the ordos plateau. China J Arid Env 74(4):498–507

    Google Scholar 

  • Zhang Y, Wang X, Zhen Y, Mi T, He H, Yu Z (2017) Microbial diversity and community structure of sulfate-reducing and sulfur-oxidizing bacteria in sediment cores from the east China sea. Front Microb 8:2133

    Google Scholar 

  • Zumft WG (1993) The biological role of nitric oxide in bacteria. Arch Microb 160(4):253–264

    CAS  Google Scholar 

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Acknowledgements

This article acknowledges the funding support provided by the National Key Research and Development Program of China (No. 2020YFA0906800) and National Science Foundation of China (Nos. 31872633, 21878307 and 31800030).

Funding

Key Research and Development Program of Jiangxi Province, 2020YFA0906800, Jianmin Xing, National Natural Science Foundation of China, 31872633, Maohua Yang.

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Authors and Affiliations

  1. CAS Key Laboratory of Green Process and Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing, 100190, China

    Xiangyuan Li, Maohua Yang, Tingzhen Mu, Delu Miao & Jianmin Xing

  2. College of Bioscience and Bioengineering, Hebei University of Science and Technology, Shijiazhuang, 050018, Hebei, China

    Xiangyuan Li & Jinlong Liu

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Contributions

MHY and JMX designed the experiment and wrote the first draft. XYL, ZXL, TZM, DLM, and JLL collected the fecal samples and performed preliminary preparation. All authors have helped in revision and approved the final manuscript.

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Correspondence to Maohua Yang.

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Li, X., Yang, M., Mu, T. et al. Composition and key-influencing factors of bacterial communities active in sulfur cycling of soda lake sediments. Arch Microbiol 204, 317 (2022). https://doi.org/10.1007/s00203-022-02925-7

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