Abstract
Hypersaline lakes and saltern areas are important industrial and biodiversity resources in the Qaidam Basin of China that reside at > 2600 m asl. Most hypersaline environments in this area are characterized by saturated salinity (~ 300 g/L salinity), nearly neutral pH, intense ultraviolet radiation, and extremely variable temperature fluctuations. The core bacterial communities associated with these stressful environments have nevertheless remained uninvestigated. 16S rRNA gene Illumina sequencing analyses revealed that the bacterial communities were dominated by core lineages including the Proteobacteria (39.4–64.6%) and the Firmicutes (17.0–42.7%). However, the relative abundances of common lineages, and especially the five most abundant taxa of Pseudomonas, Lactococcus, Anoxybacillus, Acinetobacter, and Brevundimonas, were highly variable across communities and closely associated with hypersaline characteristics in the samples. Network analysis revealed the presence of co-occurrence high relative abundance taxa (cluster I) that were highly correlated across all hypersaline samples. Additionally, temperature, total organic carbon, K+, and Mg2+ correlated highest with taxonomic distributions across communities. These results highlight the potential mechanisms that could underlie survival and adaptation to these extreme hypersaline ecosystems.
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References
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
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
Baxter BK (2018) Great Salt Lake microbiology: a historical perspective. Int Microbiol 21:79–95
Bodaker I, Sharon I, Suzuki MT, Feingersch R, Shmoish M, Andreishcheva E, Sogin ML, Rosenberg M, Maguire ME, Belkin S, Oren A, Béjà O (2010) Comparative community genomics in the dead sea: an increasingly extreme environment. ISME J 4:399–407
Bolotin A, Wincker P, Mauger S, Jaillon O, Malarme K, Weissenbach J, Ehrlich SD, Sorokin A (2001) The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res 11:731–753
Cabestrero Ó, Sanz-Montero ME, Arregu L, Serrano S, Visscher PT (2018) Seasonal variability of mineral formation in microbial mats subjected to drying and wetting cycles in alkaline and hypersaline sedimentary environments. Aquat Geochem 24:79–105
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
Çınar S, Mutlu MB (2016) Comparative analysis of prokaryotic diversity in solar salterns in eastern Anatolia (Turkey). Extremophiles 20:589–601
de la Haba RR, Sánchez-Porro C, Marquez MC, Ventosa A (2010) Extremophiles halophiles: taxonomy of halophiles. In: Stetter KO (ed) Extremophiles Handbook. Springer, Berlin Heidelberg Germany, pp 255–308
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200
Edwardson CF, Hollibaugh JT (2018) Composition and activity of microbial communities along the redox gradient of an alkaline, hypersaline, lake. Front Microbiol 9:14
Fazi S, Butturini A, Tassi F, Amalfitano S, Venturi S, Vazquez E, Clokie M, Wanjala SW, Pacini N, Harper DM (2018) Biogeochemistry and biodiversity in a network of saline-alkaline lakes: implications of ecohydrological connectivity in the kenyan rift valley. Ecohydrol Hydrobiol 18:96–106
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
Gomariz M, Martínez-García M, Santos F, Rodriguez F, Capella-Gutiérrez S, Gabaldón T, Rosselló-Móra R, Meseguer I, Antón J (2015) From community approaches to single-cell genomics: the discovery of ubiquitous hyperhalophilic bacteroidetes generalists. ISME J 9:16–31
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
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
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
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
Jiang H, Huang J, Yang J (2018) Halotolerant and halophilic microbes and their environmental implications in saline and hypersaline lakes in Qinghai province, China. In: Li WJ (ed) Extremophiles in Eurasian ecosystems: ecology, diversity, and applications. Springer, Singapore, pp 299–316
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
Kimbrel JA, Nicholas B, Yu-Wei W, David MM, Hazen TC, Simmons BA, Singer SW, Jansson JK (2018) Microbial community structure and functional potential along a hypersaline gradient. Front Microbiol 9:1492
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
Liu W, Jiang H, Yang J, Wu G (2018) Gammaproteobacterial diversity and carbon utilization in response to salinity in the lakes on the Qinghai-tibetan plateau. Geomicrobiol J 35:392–403
Liu Y, Priscu JC, Xiong J (2016) Salinity drives archaeal distribution patterns in high altitude lake sediments on the Tibetan Plateau. FEMS Microbiol Ecol 92:033
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
Martin M (2011) CUTADAPT removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12
Máthé I, Borsodi AK, Tóth EM, Felföldi T, Jurecska L, Krett G, Kelemen Z, Elekes E, Barkács K, Márialigeti K (2014) Vertical physico-chemical gradients with distinct microbial communities in the hypersaline and heliothermal lake Ursu (Sovata, Romania). Extremophiles 18:501–514
McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297
Mcgenity TJ, Oren A (2012) Hypersaline environments. In: Bell EM (ed) Life at extremes environments organisms and strategies for survival. CAB International, Dunbeg, pp 402–437
Mianping Z (2014) Classification of saline lakes and types of mineral deposit. In: Mianping Z (ed) An introduction to Saline Lakes on the Qinghai-Ttibet Plateau. Springer, Dordrecht, pp 79–84
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 77:558
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
Naghoni A, Emtiazi G, Amoozegar MA, Cretoiu MS, Stal LJ, Etemadifar Z, Fazeli SA, Bolhuis H (2017) Microbial diversity in the hypersaline Lake Meyghan. Iran Sci Rep 7:11522
Paul D, Kumbhare SV, Mhatre SS, Chowdhury SP, Shetty SA, Marathe NP, Bhute S, Shouche YS (2016) Exploration of microbial diversity and community structure of Lonar Lake: the only hypersaline meteorite crater lake within basalt rock. Front Microbiol 6:1553
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
Saraoui T, Leroi F, Björkroth J, Pilet MF (2016) Lactococcus piscium: a psychotrophic lactic acid bacterium with bioprotective or spoilage activity in food—a review. J Appl Microbiol 121:907–918
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
Schmidt TS, Matias Rodrigues JF, Mering CV (2017) A family of interaction-adjusted indices of community similarity. ISME J 11:791–807
Sirisena KA, Ramirez S, Steele A, Glamoclija M (2018) Microbial diversity of hypersaline sediments from Lake Lucero playa in white sands national monument, new Mexico, USA. Microb Ecol 76:404–418
Ventosa A, de la Haba RR, Sánchez-Porro C, Papke RT (2015) Microbial diversity of hypersaline environments: a metagenomic approach. Curr Opin Microbiol 25:80–87
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
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267
Wei Z, Hu X, Li X, Zhang Y, Jiang L, Li J, Guan Z, Cai Y, Liao X (2017) The rhizospheric microbial community structure and diversity of deciduous and evergreen forests in Taihu Lake area. China PLoS One 12:e0174411
Williams RJ, Howe A, Hofmockel KS (2014) Demonstrating microbial co-occurrence pattern analyses within and between ecosystems. Front Microbiol 5:358
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
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 35:1–7
Yang J, Ma L, Jiang H, Wu G, Dong H (2016) Salinity shapes microbial diversity and community structure in surface sediments of the Qinghai-Tibetan lakes. Sci Rep 6:25078
Yau S, Lauro FM, Williams TJ, Demaere MZ, Brown MV, Rich J, Gibson JA, Cavicchioli R (2013) Metagenomic insights into strategies of carbon conservation and unusual sulfur biogeochemistry in a hypersaline antarctic lake. ISME J 7:1944–1961
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
Zheng M, Liu X (2009) Hydrochemistry of salt lakes of the Qinghai-tibet Plateau, China. Aquat Geochem 15:293–320
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
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 2018ZJ778, 2018ZJ930Q, and 2020ZJ767, as well as the Team’s Research Program of Microbial Resources in Salt-lakes of Qinghai-Tibetan Plateau grant number 2018KYT1. We thank Accdon (www.accdon.com) and LetPub (www.letpub.com) for providing linguistic assistance during the preparation of this manuscript.
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DZ performed most of the experiments, data interpretation, and wrote the manuscript. RW supervised the execution of the experiments, analyzed the data, and wrote the manuscript. QH, QL, and XG performed the sample collection. JX, GS, and YL provided the bioinformatics technical assistance, evaluated the data, and wrote the manuscript. All authors read and approved the final version of manuscript.
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Zhu, D., Han, R., Long, Q. et al. An evaluation of the core bacterial communities associated with hypersaline environments in the Qaidam Basin, China. Arch Microbiol 202, 2093–2103 (2020). https://doi.org/10.1007/s00203-020-01927-7
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DOI: https://doi.org/10.1007/s00203-020-01927-7