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Poorly known microbial taxa dominate the microbiome of hypersaline Sambhar Lake salterns in India

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Abstract

Inland athalassohaline solar salterns provide unique opportunity to study microbial successions along salinity gradients that resemble transition in natural hypersaline lakes. We analyzed for the first time 16S rRNA gene amplicon sequences of bacteria (V1–V2) and archaea (V4–V5) in saltern brines of India’s largest inland hypersaline Sambhar Lake. Brines of the salterns (S1–S4) are alkaline (pH 9.5–10.5) with salinities of 130, 170, 280 and 350 gL−1 respectively. 16S rRNA gene copy-number of archaea outnumbered that of bacteria in all salterns. Their diversity also increased along S1 through S4, while that of bacteria decreased. Brines of S3 and S4 were dominated by specialized extreme halophilic bacterial (Halanaerobiales, Rhodothermaceae) and archaeal (Halobacteriales, Haloferacales) members with recognized salt-in strategy for osmoadaptation. Microbial assemblages positively correlated to saltern pH, total salinity, and ionic composition. Archaea in S1 and S2 were unprecedentedly represented by poorly known as-yet uncultivated groups, Woesearchaeota (90.35–93.51%) and Nanohaloarchaeota that belong to the newly proposed nano-sized superphylum DPANN. In fact, these taxa were identified in archaeal datasets of other athalassohaline salterns after re-analysis using latest RDP database. Thus, microbial compositions in hypersaline lakes are complex and need revisit particularly for their archaeal diversity to understand their hitherto unknown ecological function in extreme environments.

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References

  • Andrei AŞ, Banciu HL, Oren A (2012) Living with salt: metabolic and phylogenetic diversity of archaea inhabiting saline ecosystems. FEMS Microbiol Lett 330:1–9

    CAS  PubMed  Google Scholar 

  • Andrei A-Ş, Robeson MS, Baricz A, Coman C, Muntean V, Ionescu A, Etiope G, Alexe M, Sicora CI, Podar M, Banciu HL (2015) Contrasting taxonomic stratification of microbial communities in two hypersaline meromictic lakes. ISME J 9:2642–2656

    PubMed  PubMed Central  Google Scholar 

  • Baati H, Guermazi S, Amdouni R, Gharsallah N, Sghir A, Ammar EJE (2008) Prokaryotic diversity of a Tunisian multipond solar saltern. Extremophiles 12:505–518

    CAS  PubMed  Google Scholar 

  • Baker G, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55:541–555

    CAS  PubMed  Google Scholar 

  • Banerjee S, Sar A, Misra A, Pal S, Chakraborty A, Dam B (2018) Increased productivity in poultry birds by sub-lethal dose of antibiotics is arbitrated by selective enrichment of gut microbiota, particularly short-chain fatty acid producers. Microbiology 164:142–153

    CAS  PubMed  Google Scholar 

  • Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2009) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267

    PubMed  PubMed Central  Google Scholar 

  • 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 7:335

    CAS  PubMed  PubMed Central  Google Scholar 

  • Castelle CJ, Wrighton KC, Thomas BC, Hug LA, Brown CT, Wilkins MJ, Frischkorn KR, Tringe SG, Singh A, Markillie LM (2015) Genomic expansion of domain archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. Curr Biol 25:690–701

    CAS  PubMed  Google Scholar 

  • Cherekar MN, Pathak AP (2015) Studies on haloalkaliphilic gammaproteobacteria from hypersaline Sambhar Lake, Rajasthan, India. Indian J Mar Sci 44:1646–1653

    Google Scholar 

  • Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM (2013) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42:D633–D642

    PubMed  PubMed Central  Google Scholar 

  • Durbin AM, Teske A (2010) Sediment-associated microdiversity within the Marine Group I Crenarchaeota. Environ Microbiol Rep 2:693–703

    CAS  PubMed  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    CAS  PubMed  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996

    CAS  PubMed  Google Scholar 

  • Emerson JB, Andrade K, Thomas BC, Norman A, Allen EE, Heidelberg KB, Banfield JF (2013) Virus-host and CRISPR dynamics in Archaea-dominated hypersaline Lake Tyrrell, Victoria, Australia. Archaea 2013:370871

    PubMed  PubMed Central  Google Scholar 

  • Ghai R, Pašić L, Fernández AB, Martin-Cuadrado A-B, Mizuno CM, McMahon KD, Papke RT, Stepanauskas R, Rodriguez-Brito B, Rohwer F, Sánchez-Porro C, Ventosa A, Rodríguez-Valera F (2011) New abundant microbial groups in aquatic hypersaline environments. Sci Rep 1:135

    PubMed  PubMed Central  Google Scholar 

  • Grant W, Mwatha W, Jones B (1990) Alkaliphiles: ecology, diversity and applications. FEMS Microbiol Lett 75:255–269

    CAS  Google Scholar 

  • Grant S, Grant WD, Jones BE, Kato C, Li L (1999) Novel archaeal phylotypes from an East African alkaline saltern. Extremophiles 3:139–145

    CAS  PubMed  Google Scholar 

  • Hamm JN, Erdmann S, Eloe-Fadrosh EA, Angeloni A, Zhong L, Brownlee C, Williams TJ, Barton K, Carswell S, Smith MA (2019) Unexpected host dependency of Antarctic Nanohaloarchaeota. Proc Natl Acad Sci U S A 116:14661–14670

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hammer Ø, Harper DA, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electronica 4:9

    Google Scholar 

  • Han R, Zhang X, Liu J, Long Q, Chen L, Liu D, Zhu D (2017) Microbial community structure and diversity within hypersaline Keke Salt Lake environments. Can J Microbiol 63:895–908

    CAS  PubMed  Google Scholar 

  • Koskinen K, Pausan MR, Perras AK, Beck M, Bang C, Mora M, Schilhabel A, Schmitz R, Moissl-Eichinger C (2017) First insights into the diverse human archaeome: specific detection of archaea in the gastrointestinal tract, lung, and nose and on skin. MBio 8:e00824–e1817

    CAS  PubMed  PubMed Central  Google Scholar 

  • La Cono V, Messina E, Rohde M, Arcadi E, Ciordia S, Crisafi F, Denaro R, Ferrer M, Giuliano L, Golyshin PN (2019) Differential polysaccharide utilization is the basis for a nanohaloarchaeon: haloarchaeon symbiosis. Biorxiv. https://doi.org/10.1101/794461:794461

    Article  Google Scholar 

  • Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Thurber RLV, Knight R (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Li M, Castelle CJ, Probst AJ, Zhou Z, Pan J, Liu Y, Banfield JF, Gu J-D (2018) Insights into the ecology, evolution, and metabolism of the widespread Woesearchaeotal lineages. Microbiome 6:102

    PubMed  PubMed Central  Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet 17:10–12

    Google Scholar 

  • Mesbah NM, Abou-El-Ela SH, Wiegel J (2007) Novel and unexpected prokaryotic diversity in water and sediments of the alkaline, hypersaline lakes of the Wadi An Natrun. Egypt Microb Ecol 54:598–617

    CAS  PubMed  Google Scholar 

  • Narasingarao P, Podell S, Ugalde JA, Brochier-Armanet C, Emerson JB, Brocks JJ, Heidelberg KB, Banfield JF, Allen EE (2012) De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities. ISME J 6:81

    CAS  PubMed  Google Scholar 

  • Neelam DK, Agrawal A, Tomer AK, Bandyopadhayaya S, Sharma A, Jagannadham MV, Mandal CC, Dadheech PK (2019) A Piscibacillus sp isolated from a soda lake exhibits anticancer activity against breast cancer MDA-MB-231 cells. Microorganisms 7:34

    CAS  PubMed Central  Google Scholar 

  • Ochsenreiter T, Selezi D, Quaiser A, Bonch-Osmolovskaya L, Schleper CJEM (2003) Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR. Environ Microbiol 5:787–797

    CAS  PubMed  Google Scholar 

  • Oldham AL, Duncan KE (2012) Similar gene estimates from circular and linear standards in quantitative PCR analyses using the prokaryotic 16S rRNA Gene as a Model. PLoS ONE 7:e51931. https://doi.org/10.1371/journal.pone.0051931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oren A (2008) Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Syst 4:2

    PubMed  PubMed Central  Google Scholar 

  • Oren A (2014) Halophilic archaea on Earth and in space: growth and survival under extreme conditions. Philos Trans A Math Phys Eng Sci 372:20140194

    PubMed  Google Scholar 

  • Oren A, Heldal M, Norland S, Galinski EA (2002) Intracellular ion and organic solute concentrations of the extremely halophilic bacterium Salinibacter ruber. Extremophiles 6:491–498

    CAS  PubMed  Google Scholar 

  • Ortiz-Alvarez R, Casamayor EO (2016) High occurrence of Pacearchaeota and Woesearchaeota (Archaea superphylum DPANN) in the surface waters of oligotrophic high-altitude lakes. Environ Microbiol Rep 8:210–217

    CAS  PubMed  Google Scholar 

  • Pagaling E, Wang H, Venables M, Wallace A, Grant WD, Cowan DA, Jones BE, Ma Y, Ventosa A, Heaphy S (2009) Microbial biogeography of six salt lakes in Inner Mongolia, China, and a salt lake in Argentina. Appl Environ Microbiol 75:5750–5760

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pal S, Sar A, Dam B (2019) Moderate halophilic bacteria, but not extreme halophilic archaea can alleviate the toxicity of short-alkyl side chain imidazolium-based ionic liquids. Ecotoxicol Environ Saf 184:109634. https://doi.org/10.1016/j.ecoenv.2019.109634

    Article  CAS  PubMed  Google Scholar 

  • Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shcherbakova V, Yoshimura Y, Ryzhmanova Y, Taguchi Y, Segawa T, Oshurkova V, Rivkina E (2016) Archaeal communities of Arctic methane-containing permafrost. FEMS Microbiol Ecol 92:9

    Google Scholar 

  • Sinha R, Raymahashay B (2004) Evaporite mineralogy and geochemical evolution of the Sambhar Salt Lake, Rajasthan, India. Sediment Geol 166:59–71

    CAS  Google Scholar 

  • Soppa J (2011) Ploidy and gene conversion in Archaea. Biochem SocTrans 39:150–154

    CAS  Google Scholar 

  • Sorokin DY, Berben T, Melton ED, Overmars L, Vavourakis CD, Muyzer G (2014) Microbial diversity and biogeochemical cycling in soda lakes. Extremophiles 18:791–809

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun D-L, Jiang X, Wu QL, Zhou N-Y (2013) Intragenomic heterogeneity of 16S rRNA genes causes overestimation of prokaryotic diversity. Appl Environ Microbiol 79:5962–5969

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takai K, Horikoshi K (1999) Genetic diversity of archaea in deep-sea hydrothermal vent environments. Genetics 152:1285–1297

    CAS  PubMed  PubMed Central  Google Scholar 

  • Upasani V, Desai S (1990) Sambhar salt lake. Arch Microbiol 154:589–593

    CAS  Google Scholar 

  • Vaisman N, Oren A (2009) Salisaeta longa gen. nov., sp. nov., a red, halophilic member of the Bacteroidetes. Int J Syst Evol Microbiol 59:2571–2574

    CAS  PubMed  Google Scholar 

  • Vavourakis CD, Ghai R, Rodriguez-Valera F, Sorokin DY, Tringe SG, Hugenholtz P, Muyzer G (2016) Metagenomic insights into the uncultured diversity and physiology of microbes in four hypersaline soda lake brines. Front Microbiol 7:211

    PubMed  PubMed Central  Google Scholar 

  • Ventosa A, Fernández AB, León MJ, Sánchez-Porro C, Rodriguez-Valera FJE (2014) The Santa Pola saltern as a model for studying the microbiota of hypersaline environments. Extremophiles 18:811–824

    CAS  PubMed  Google Scholar 

  • Xie W, Zhang C, Zhou X, Wang PJAm, biotechnology, (2014) Salinity-dominated change in community structure and ecological function of Archaea from the lower Pearl River to coastal South China Sea. Appl Microbiol Biotechnol 98:7971–7982

    CAS  PubMed  Google Scholar 

  • Yadav AN, Verma P, Kumar M, Pal KK, Dey R, Gupta A, Padaria JC, Gujar GT, Kumar S, Suman A (2015) Diversity and phylogenetic profiling of niche-specific Bacilli from extreme environments of India. Ann Microbiol 65:611–629

    Google Scholar 

  • Zerulla K, Soppa J (2014) Polyploidy in haloarchaea: advantages for growth and survival. Front Microbiol 5:274

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was financially supported by CSIR [No. 38(1410)/15/ EMR-II)]. Srikanta Pal, Sohini Banerjee and Puja Mukherjee are grateful to CSIR; Abhijit Sar to UGC-BSR; and Raju Biswas to WB-DST for their respective fellowships. We would thank the editors and two eminent unanimous reviewers whose inputs and suggestions have immensely improved the overall scientific quality of the final version of the manuscript.

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Authors and Affiliations

  1. Microbiology Laboratory, Department of Botany (DST-FIST and UGC-DRS Funded), Institute of Science, Visva-Bharati (A Central University), Santiniketan, West Bengal, 731235, India

    Srikanta Pal, Raju Biswas, Arijit Misra, Abhijit Sar, Sohini Banerjee, Puja Mukherjee & Bomba Dam

  2. Present address: Department of Obstetrics and Gynecology, Division of Maternal-Fetal Medicine, Baylor College of Medicine, Houston, TX, USA

    Sohini Banerjee

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  1. Srikanta Pal
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Pal, S., Biswas, R., Misra, A. et al. Poorly known microbial taxa dominate the microbiome of hypersaline Sambhar Lake salterns in India. Extremophiles 24, 875–885 (2020). https://doi.org/10.1007/s00792-020-01201-0

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