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Distinctive distributions of halophilic Archaea across hypersaline environments within the Qaidam Basin of China

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Abstract

Halophilic Archaea are widely distributed globally in hypersaline environments. However, little is known of how dominant halophilic archaeal genera are distributed across environments and how they may co-associate across ecosystems. Here, the archaeal community composition and diversity from hypersaline environments (> 300 g/L salinity; total of 33 samples) in the Qaidam Basin of China were investigated using high-throughput Illumina sequencing of 16S rRNA genes. The archaeal communities (total of 3,419 OTUs) were dominated by the class Halobacteria (31.7–99.6% relative abundances) within the phylum Euryarchaeota (90.8–99.9%). Five predominant taxa, including Halorubrum, Halobacterium, Halopenitus, Methanothrix, and Halomicrobium, were observed across most samples. However, several distinct genera were associated with individual samples and were inconsistently distributed across samples, which contrast with previous studies of hypersaline archaeal communities. Additionally, co-occurrence network analysis indicated that five network clusters were present and potentially reflective of interspecies interactions among the environments, including three clusters (clusters II, III, and IV) comprising halophilic archaeal taxa within the Halobacteriaceae and Haloferacaceae families. In addition, two other clusters (clusters I and V) were identified that comprised methanogens. Finally, salinity comprising ionic concentrations (in the order of Na+ > Ca2+ > Mg2+) and pH were most correlated with taxonomic distributions across sample sites.

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References

  • Abdallah MB, Karray F, Mhiri N, Mei N, Quéméneur M, Cayol JL, Erauso G, Tholozan JL, Alazard D, Sayadi S (2016) Prokaryotic diversity in a Tunisian hypersaline lake, Chott El Jerid. Extremophiles 20:125–138

    Article  PubMed  CAS  Google Scholar 

  • Abdallah MB, Karray F, Kallel N, Armougom F, Mhiri N, Quéméneur M, Cayol JL, Erauso G, Sayadi S (2018) Abundance and diversity of prokaryotes in ephemeral hypersaline lake Chott El Jerid using Illumina Miseq sequencing, DGGE and qPCR assays. Extremophiles 22:811–823

    Article  PubMed  CAS  Google Scholar 

  • Adhikari NP, Adhikari S, Liu XB, Shen L, Gu Z (2019) Bacterial diversity in alpine lakes: a review from the third pole region. J Earth Sci 30:387–396

    Article  CAS  Google Scholar 

  • Andrei AS, 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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) Qiime allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen S, Xu Y, Helfant L (2020) Geographical isolation, buried depth, and physicochemical traits drive the variation of species diversity and prokaryotic community in three typical hypersaline environments. Microorganisms 8:120

    Article  CAS  PubMed Central  Google Scholar 

  • Çınar S, Mutlu MB (2016) Comparative analysis of prokaryotic diversity in solar salterns in eastern Anatolia (Turkey). Extremophiles 20:589–601

    PubMed  Google Scholar 

  • Couto-Rodríguez RL, Montalvo-Rodríguez R (2019) Temporal analysis of the microbial community from the crystallizer ponds in Cabo Rojo, Puerto Rico, using metagenomics. Genes 10:422

    Article  PubMed Central  CAS  Google Scholar 

  • de la Haba RR, Sánchez-Porro C, Marquez MC, Ventosa A (2010) Extremophiles halophiles: taxonomy of halophiles. In: Horikoshi K, Antranikian G, Bull AT, Robb FT, Stetter KO (eds) Extremophiles Handbook. Springer, Berlin Heidelberg, Germany, pp 255–308

    Google Scholar 

  • Deng Y, Liu Y, Dumont M, Conrad R (2017) Salinity affects the composition of the aerobic Methanotroph community in alkaline lake sediments from the Tibetan Plateau. Microb Ecol 73:101–110

    Article  PubMed  Google Scholar 

  • Dillon JG, Carlin M, Gutierrez A, NguyenV, and Mclain N, (2013) Patterns of microbial diversity along a salinity gradient in the Guerrero Negro solar saltern, Baja CA Sur. Mexico Front Microbiol 4:399

    PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) Uchime improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • García-Maldonado JQ, Alejandra EZ, Luciana R, Bebout BM, Alejandro SF, Alejandro LC (2018) Bacterial and archaeal profiling of hypersaline microbial mats and endoevaporites, under natural conditions and methanogenic microcosm experiments. Extremophiles 22:903–916

    Article  PubMed  CAS  Google Scholar 

  • Ghai R, Pašić L, Fernández AB, Martin-Cuadrado AB, 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Haferburg G, Janosch AD, Schmidt GN, Kummer NA, Erquicia JC, Schlömann M (2017) Microbial diversity of the hypersaline and lithium-rich Salar de Uyuni, Bolivia. Microbiol Res 199:19–28

    Article  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, Brazendale S, Hancock AM, Allen MA, Raftery MJ, Cavicchioli R (2019) Unexpected host dependency of Antarctic Nanohaloarchaeota. PNAS 116:14661–14670

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Hayden CJ, Beman JM (2016) Microbial diversity and community structure along a lake elevation gradient in Yosemite National Park, California, USA. Environ Microbiol 18:1782–1791

    Article  PubMed  Google Scholar 

  • Hu A, Yao DD, Jiao NZ, Liu YQ, Yang Z, Liu XB (2010) Community structures of ammonia-oxidising Archaea and Bacteria in high-altitude lakes on the Tibetan Plateau. Freshwater Biol 55:2375–2390

    Article  CAS  Google Scholar 

  • Jacob JH, Hussein EI, Shakhatreh MAK, Cornelison CT (2017) Microbial community analysis of the hypersaline water of the Dead Sea using high-throughput amplicon sequencing. Microbiologyopen 6:e00500

    Article  PubMed Central  CAS  Google Scholar 

  • Jiang H, Dong H, Yu B, Liu X, Li Y, Ji S, Zhang CL (2007) Microbial response to salinity change in Lake Chaka, a hypersaline lake on Tibetan plateau. Environ Microbiol 9:2603–2621

    Article  CAS  PubMed  Google Scholar 

  • Jiang H, Dong H, Deng S, Yu B, Huang Q, Wu Q (2009) Response of archaeal community structure to environmental changes in lakes on the Tibetan Plateau, northwestern China. Geomicrobiol J 26:289–297

    Article  CAS  Google Scholar 

  • Jiang H, Huang Q, Deng S, Dong H, Yu B (2010) Planktonic actinobacterial diversity along a salinity gradient of a river and five lakes on the Tibetan Plateau. Extremophiles 14:367–376

    Article  PubMed  Google Scholar 

  • Letunic I, Bork P (2015) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 44:242–245

    Article  CAS  Google Scholar 

  • Liu Y, Yao T, Zhu L, Jiao N, Liu X, Zeng Y, Jiang HC (2009) Bacterial diversity of freshwater alpine lake Puma Yumco on the Tibetan Plateau. Geomicrobiol J 26:131–145

    Article  CAS  Google Scholar 

  • Liu Y, Priscu JC, Yao T, Vick-Majors TJ, Michaud AB, Jiao N, Hou J, Tian L, Hu A, Chen ZQ (2014) A comparison of pelagic, littoral, and riverine bacterial assemblages in lake Bangongco, Tibetan Plateau. FEMS Microbiol Ecol 89:211–221

    Article  CAS  PubMed  Google Scholar 

  • Liu K, Liun Y, JiaoN ZhuL, Wang J, Hu A, Liu X (2016a) Vertical variation of bacterial community in Nam Co, a large stratified lake in central Tibetan Plateau. Anton Leeuw 109:1323–1335

    Article  CAS  Google Scholar 

  • Liu Y, Priscu JC, Xiong J, Conrad R, Vick-Majors T, Chu H, Hou J (2016a) Salinity drives archaeal distribution patterns in high altitude lake sediments on the Tibetan Plateau. FEMS Microbiol Ecol 92:fiw033.

  • Liu W, Jiang H, Jian Y, Wu G (2018a) Gammaproteobacterial diversity and carbon utilization in response to salinity in the lakes on the Qinghai-Tibetan Plateau. Geomicrobiol J 35:392–403

    Article  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma B, Wang Y, Ye S, Liu S, Stirling E, Gilbert JA, Faust K, Knight R, Jansson JK, Cardona C, Röttjers L, Xu J (2020) Earth microbial co-occurrence network reveals interconnection pattern across microbiomes. Microbiome 8:82

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Mateu MS, Ontiveros VJ, Xavier TM, David A, Casamayor EO (2020) Dynamics and ecological distributions of the Archaea microbiome from inland saline lakes (monegros desert, Spain). FEMS Microbiol Ecol 96:fiaa019.

  • McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297

    Article  Google Scholar 

  • Mikhailov IS, Zakharova YR, Bukin YS, Galachyants YP, Petrova DP, Sakirko MV, Likhoshway YV (2019) Co-occurrence networks among bacteria and microbial eukaryotes of Lake Baikal during a spring phytoplankton bloom. Microb Ecol 77:96–109

    Article  PubMed  Google Scholar 

  • Milici M, Deng ZL, Tomasch J, Decelle J, Wos-Oxley ML, Wang H, Jáuregui R, Plumeier I, Giebel HA, Badewien TH, Wurst M, Pieper DH, Simon M, Wagner-Döbler I (2016) Co-occurrence analysis of microbial taxa in the Atlantic Ocean reveals high connectivity in the free-living bacterioplankton. Front Microbiol 7:649

    PubMed  PubMed Central  Google Scholar 

  • Mora-Ruiz MR, Cifuentes A, Font-Verdera F, Pérez-Fernández C, Farias ME, González B, Orfila A, Rosselló-Móra R (2018) Biogeographical patterns of bacterial and archaeal communities from distant hypersaline environments. Syst Appl Microbiol 41:139–150

    Article  PubMed  Google Scholar 

  • Naghoni A, Emtiazi G, Amoozegar MA, Cretoiu MS, Stal LJ, Etemadifar Z, Fazeli SAS, Bolhuis H (2017) Microbial diversity in the hypersaline Lake Meyghan. Iran Sci Rep 7:11522

    Article  PubMed  CAS  Google Scholar 

  • Najjari A, Elshahed MS, Cherif A, Youssef NH (2015) Patterns and determinants of halophilic Archaea (class Halobacteria) diversity in Tunisian endorheic salt lakes and sebkhet systems. Appl Environ Microbiol 81:4432–4441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oren A (2013) Life at high salt and low oxygen: how do the halobacteriaceae cope with low oxygen concentrations in their environment. In: Seckbach J, Oren A, Stan-Lotter H (eds) Polyextremophiles: life under multiple forms of stress. Springer, Dordrecht, Netherlands, pp 531–548

    Chapter  Google Scholar 

  • Oren A (2014) Halophilic Archaea on earth and in space: growth and survival under extreme conditions. Philos Trans R Soc A 372:20140194

    Article  CAS  Google Scholar 

  • Oren A (2018) Halorubrum. In: Rainey F, Kämpfer P, Trujillo M, Chun J, DeVos P, Hedlund B, Dedysh S (eds) Whitman WB. Bergey’s Manual of Systematics of Archaea and Bacteria. John Wiley & Sons Ltd, Chichester, pp 1–48

    Google Scholar 

  • Oren A (2019) Euryarchaeota. In: Gemmell RT, Grant WD, Stan-Lotter H (eds) McGenity TJ. Bergey’s Manual of Systematics of Archaea and Bacteria. John Wiley & Sons Ltd, Chichester, pp 1–15

    Google Scholar 

  • Oren A, Ventosa A (2016) International committee on systematic of prokaryotes subcommittee on the taxonomy of Halobacteriaceae and subcommittee on the taxonomy of Halomonadaceae. Int J Syst Evol Microbiol 66:4291–4295

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Plominsky AM, Henríquez-Castillo C, Delherbe N, Podell S, Ramirez-Flandes S, Ugalde JA, Santibañez JF, van den Engh G, Hanselmann K, Ulloa O, De la Iglesia R, Allen EE, Trefault N (2018) Distinctive archaeal composition of an artisanal crystallizer pond and functional insights into salt-saturated hypersaline environment adaptation. Front Microbiol 9:1800

    Article  PubMed  PubMed Central  Google Scholar 

  • Qin H, Wang S, Feng K, He Z, Virta MPJ, Hou W, Dong H, Ye D (2019) Unraveling the diversity of sedimentary sulfate-reducing prokaryotes (SRP) across Tibetan saline lakes using epicPCR. Microbiome 7:71

    Article  PubMed  PubMed Central  Google Scholar 

  • Qu X, Zhang M, Yang Y, Xie Y, Ren Z, Peng W, Du X (2019) Taxonomic structure and potential nitrogen metabolism of microbial assemblage in a large hypereutrophic steppe lake. Environ Sci Pollut R 26:21151–21160

    Article  CAS  Google Scholar 

  • Ren Z, Wang F, Qu X, Elser JJ, Liu Y, Chu L (2017) Taxonomic and functional differences between microbial communities in Qinghai Lake and its input streams. Front Microbiol 8:2319

    Article  PubMed  PubMed Central  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt TS, Matias Rodrigues JF, Mering CV (2017) A family of interaction-adjusted indices of community similarity. ISME J 11:791–807

    Article  PubMed  Google Scholar 

  • Segata N, Izard J, Waldron L, Gevers D, Miropolskyn L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60

    Article  PubMed  PubMed Central  Google Scholar 

  • Shi Y, Fan K, Li Y, Yang T, Chu H (2019) Archaea enhance the robustness of microbial co-occurrence networks in Tibetan Plateau soils. Soil Sci Soc Am J 83:1093–1099

    Article  CAS  Google Scholar 

  • Takai K, Horikoshi K (2000) Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66:5066–5072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vavourakis CD, Andrei AS, Mehrshad M, Ghai R, Sorokin DY, Muyzer G (2018) A metagenomics roadmap to the uncultured genome diversity in hypersaline soda lake sediments. Microbiome 6:168

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Xiong J, Liu Y, Lin X, Zhang H, Zeng J, Hou J, Yang Y, Yao T, Knight R, Chu H (2012) Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan Plateau. Environ Microbiol 14:2457–2466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang J, Jiang H, Dong H, Wang H, Wu G, Hou W, Liu W, Zhang C, Sun Y, Lai Z (2013) Amoza-encoding Archaea and thaumarchaeol in the lakes on the northeastern Qinghai-Tibetan Plateau. China Front Microbiol 4:329

    CAS  PubMed  Google Scholar 

  • Yang J, Jiang H, Wu G, Liu W (2018) Phylum-level archaeal distributions in the sediments of Chinese lakes with a large range of salinity. Geomicrobiol J 35:404–410

    Article  CAS  Google Scholar 

  • Yang J, Jiang H, Wang LW, B, (2018) Benthic algal community structures and their response to geographic distance and environmental variables in the Qinghai-Tibetan lakes with different salinity. Front Microbiol 9:578

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang J, Jiang H, Dong H, Liu Y (2019) A comprehensive census of lake microbial diversity on a global scale. Sci China Life Sci 62:1320–1331

    Article  PubMed  Google Scholar 

  • Youssef NH, Ashlock-Savage KN, Elshahed MS (2011) Phylogenetic diversities and community structure of members of the extremely halophilic Archaea (Order Halobacteriales) in multiple saline sediment habitats. Appl Environ Microbiol 78:1332–1344

    Article  PubMed  CAS  Google Scholar 

  • Zhe M, Zhang X, Wang B, Sun R, Zheng D (2017) Hydrochemical regime and its mechanism in Yamzhog Yumco Basin, south Tibet. J Geogr Sci 27:1111–1122

    Article  Google Scholar 

  • Zheng M, Liu X (2009) Hydrochemistry of salt lakes of the Qinghai-tibet Plateau, China. Aquat Geochem 15:293–320

    Article  CAS  Google Scholar 

  • Zhong ZP, Liu Y, Miao LL, Wang F, Chu LM, Wang JL, Liu ZP (2016) Prokaryotic community structure driven by salinity and ionic concentrations in plateau lakes of the Tibetan Plateau. Appl Environ Microbiol 82:1846–1858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong H, Lehtovirta-Morley L, Liu J, Zheng Y, Lin H, Song D, Todd JD, Tian J, Zhang XH (2020) Novel insights into the Thaumarchaeota in the deepest oceans: their metabolism and potential adaptation mechanisms. Microbiome 8:78

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhu D, Han R, Long Q, Gao X, Xing J, Shen G, Li Y, Wang R (2020) An evaluation of the core bacterial communities associated with hypersaline environments in the Qaidam Basin, China. Arch Microbiol 202:2093–2103

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China grant numbers 31760034, 31860030, and 21967018, in addition to the Key Research Foundation of Development and Transformation of Qinghai Province grant number 2019SF121, the Applied Basic Research Program of Qinghai Province grant numbers 2020ZJ767, and 2018ZJ930Q, as well as the Team’s Research Program of Microbial Resources in Salt-lakes of Qinghai-Tibetan Plateau grant number 2018KYT1. We would like to thank LetPub (www.letpub.com) for providing linguistic assistance during the preparation of this manuscript.

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DZ performed most of the experiments, and wrote the manuscript. GS and RW supervised the execution of the experiments, and analyzed the data. ZW, QH, QL, and XG performed the sample collection. JX, GS, and YL provided the bioinformatics technical assistance, and evaluated the data. All authors read and approved the final version of manuscript.

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Correspondence to Rong Wang.

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Zhu, D., Shen, G., Wang, Z. et al. Distinctive distributions of halophilic Archaea across hypersaline environments within the Qaidam Basin of China. Arch Microbiol 203, 2029–2042 (2021). https://doi.org/10.1007/s00203-020-02181-7

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