Differences in archaeal diversity and potential ecological functions between saline and hypersaline lakes on Qinghai-Tibet Plateau were driven by multiple environmental and non-environmental factors beyond the salinity.
Archaea
Diversity
Ecological functions
Network analysis
Plateau saline lakes
Journal
BMC microbiology
ISSN: 1471-2180
Titre abrégé: BMC Microbiol
Pays: England
ID NLM: 100966981
Informations de publication
Date de publication:
04 May 2024
04 May 2024
Historique:
received:
15
11
2023
accepted:
15
04
2024
medline:
5
5
2024
pubmed:
5
5
2024
entrez:
4
5
2024
Statut:
epublish
Résumé
Saline lakes are home to various archaea that play special and crucial roles in the global biogeochemical cycle. The Qinghai-Tibet Plateau hosts a large number of lakes with diverse salinity ranging from 0.1 to over 400 g/L, harboring complex and diverse archaea. To the best of our knowledge, the formation mechanisms and potential ecological roles of archaea in Qinghai-Tibetan Plateau saline lakes remain largely unknown. Using High-throughput Illumina sequencing, we uncovered the vastly distinct archaea communities between two typical saline lakes with significant salinity differences on the Qinghai Tibet Plateau (Qinghai saline lake and Chaka hypersaline lake) and suggested archaea played different important roles in methanogenesis-related and nitrate reduction-related functions of these two lakes, respectively. Rather than the individual effect of salinity, the composite effect of salinity with diverse environmental parameters (e.g., temperature, chlorophyll a, total nitrogen, and total phosphorus) dominated the explanation of the variations in archaeal community structure in different habitats. Based on the network analysis, we further found the correlations between dominant archaeal OTUs were tight but significantly different between the two habitats, implying that archaeal interactions may also largely determine the shape of archaeal communities. The present study improved our understanding of the structure and function of archaea in different saline lakes on the Qinghai-Tibet Plateau and provided a new perspective on the mechanisms underlying shaping their communities.
Sections du résumé
BACKGROUND
BACKGROUND
Saline lakes are home to various archaea that play special and crucial roles in the global biogeochemical cycle. The Qinghai-Tibet Plateau hosts a large number of lakes with diverse salinity ranging from 0.1 to over 400 g/L, harboring complex and diverse archaea. To the best of our knowledge, the formation mechanisms and potential ecological roles of archaea in Qinghai-Tibetan Plateau saline lakes remain largely unknown.
RESULTS
RESULTS
Using High-throughput Illumina sequencing, we uncovered the vastly distinct archaea communities between two typical saline lakes with significant salinity differences on the Qinghai Tibet Plateau (Qinghai saline lake and Chaka hypersaline lake) and suggested archaea played different important roles in methanogenesis-related and nitrate reduction-related functions of these two lakes, respectively. Rather than the individual effect of salinity, the composite effect of salinity with diverse environmental parameters (e.g., temperature, chlorophyll a, total nitrogen, and total phosphorus) dominated the explanation of the variations in archaeal community structure in different habitats. Based on the network analysis, we further found the correlations between dominant archaeal OTUs were tight but significantly different between the two habitats, implying that archaeal interactions may also largely determine the shape of archaeal communities.
CONCLUSION
CONCLUSIONS
The present study improved our understanding of the structure and function of archaea in different saline lakes on the Qinghai-Tibet Plateau and provided a new perspective on the mechanisms underlying shaping their communities.
Identifiants
pubmed: 38704527
doi: 10.1186/s12866-024-03307-3
pii: 10.1186/s12866-024-03307-3
doi:
Substances chimiques
RNA, Ribosomal, 16S
0
Nitrogen
N762921K75
DNA, Archaeal
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
153Subventions
Organisme : The National Natural Science Foundation of China
ID : 32170063
Organisme : Scientific Research and Innovation Platform Construction Project Supported by Central Funds in 2023-Scientific Research and Innovation Teams of Forestry and Grassland Ecosystem Function Maintenance and Sustainable Development and Utilization in Qinghai Province
ID : 30160101141
Organisme : Research Program of Application Foundation of Qinghai Province
ID : 2024-ZJ-749
Informations de copyright
© 2024. The Author(s).
Références
Saccò M, White NE, Harrod C, Salazar G, Aguilar P, Cubillos CF, Meredith K, Baxter BK, Oren A, Anufriieva E, et al. Salt to conserve: a review on the ecology and preservation of hypersaline ecosystems. Biol Rev. 2021;96(6):2828–50.
pubmed: 34747117
doi: 10.1111/brv.12780
Liu Y, Priscu JC, Xiong J, Conrad R, Vick-Majors T, Chu H, Hou J. Salinity drives archaeal distribution patterns in high altitude lake sediments on the Tibetan Plateau. FEMS Microbiol Ecol. 2016;92(3):fiw033.
pubmed: 26887660
doi: 10.1093/femsec/fiw033
Oren A. Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J Ind Microbiol Biotechnol. 2002;28(1):56–63.
pubmed: 11938472
doi: 10.1038/sj/jim/7000176
Margesin R, Schinner F. Potential of halotolerant and halophilic microorganisms for biotechnology. Extremophiles. 2001;5(2):73–83.
pubmed: 11354458
doi: 10.1007/s007920100184
Jiang H, Dong H, Yu B, Liu X, Li Y, Ji S, Zhang CL. Microbial response to salinity change in Lake Chaka, a hypersaline lake on tibetan plateau. Environ Microbiol. 2007;9(10):2603–21.
pubmed: 17803783
doi: 10.1111/j.1462-2920.2007.01377.x
Almeida-Dalmet S, Sikaroodi M, Gillevet PM, Litchfield CD, Baxter BK. Temporal study of the microbial diversity of the north arm of Great Salt Lake, Utah, U.S. Microorganisms. 2015; 3(3):310 – 26.
Baker BJ, De Anda V, Seitz KW, Dombrowski N, Santoro AE, Lloyd KG. Diversity, ecology and evolution of Archaea. Nat Microbiol. 2020;5(7):887–900.
pubmed: 32367054
doi: 10.1038/s41564-020-0715-z
Spang A, Caceres EF, Ettema TJG. Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life. Science. 2017;357(6351):eaaf3883.
pubmed: 28798101
doi: 10.1126/science.aaf3883
Andrei AŞ, Banciu HL, Oren A. Living with salt: metabolic and phylogenetic diversity of archaea inhabiting saline ecosystems. FEMS Microbiol Lett. 2012;330(1):1–9.
pubmed: 22339687
doi: 10.1111/j.1574-6968.2012.02526.x
Jiang H, Dong H, Deng S, Yu B, Huang Q, Wu Q. Response of archaeal community structure to environmental changes in lakes on the Tibetan Plateau, Northwestern China. Geomicrobiol J. 2009;26(4):289–97.
doi: 10.1080/01490450902892662
Zhong ZP, Liu Y, Miao LL, Wang F, Chu LM, Wang JL, Liu ZP. Prokaryotic community structure driven by salinity and ionic concentrations in plateau lakes of the Tibetan Plateau. Appl Environ Microb. 2016;82(6):1846–58.
doi: 10.1128/AEM.03332-15
Ji M, Kong W, Yue L, Wang J, Deng Y, Zhu L. Salinity reduces bacterial diversity, but increases network complexity in tibetan Plateau lakes. FEMS Microbiol Ecol. 2019;95(12):fiz190.
pubmed: 31778180
doi: 10.1093/femsec/fiz190
Stegen JC, Lin X, Fredrickson JK, Chen X, Kennedy DW, Murray CJ, Rockhold ML, Konopka A. Quantifying community assembly processes and identifying features that impose them. ISME J. 2013;7(11):2069–79.
pubmed: 23739053
pmcid: 3806266
doi: 10.1038/ismej.2013.93
Cremer J, Melbinger A, Wienand K, Henriquez T, Jung H, Frey E. Cooperation in microbial populations: theory and experimental model systems. J Mol Biol. 2019;431(23):4599–644.
pubmed: 31634468
doi: 10.1016/j.jmb.2019.09.023
Lima-Mendez G, Faust K, Henry N, Decelle J, Colin S, Carcillo F, Chaffron S, Ignacio-Espinosa JC, Roux S, Vincent F, et al. Determinants of community structure in the global plankton interactome. Science. 2015;348(6237):1262073.
pubmed: 25999517
doi: 10.1126/science.1262073
Zhou J, Song X, Zhang C-Y, Chen G-F, Lao Y-M, Jin H, Cai Z-H. Distribution patterns of microbial community structure along a 7000-mile latitudinal transect from the Mediterranean Sea across the Atlantic Ocean to the Brazilian Coastal Sea. Microb Ecol. 2018;76(3):592–609.
pubmed: 29442157
doi: 10.1007/s00248-018-1150-z
He Y, Sen B, Shang J, He Y, Xie N, Zhang Y, Zhang J, Johnson ZI, Wang G. Seasonal influence of scallop culture on nutrient flux, bacterial pathogens and bacterioplankton diversity across estuaries off the Bohai Sea Coast of Northern China. Mar Pollut Bull. 2017;124(1):411–20.
pubmed: 28779889
doi: 10.1016/j.marpolbul.2017.07.062
He C, Lin W, Zheng X, Wang C, Hu Z, Wang W. Synergistic effect of magnetite and zero-valent iron on anaerobic degradation and methanogenesis of phenol. Bioresour Technol. 2019;291:121874.
pubmed: 31377508
doi: 10.1016/j.biortech.2019.121874
Wang G, Li Q, Gao X, Wang XC. Synergetic promotion of syntrophic methane production from anaerobic digestion of complex organic wastes by biochar: performance and associated mechanisms. Bioresour Technol. 2018;250:812–20.
pubmed: 30001588
doi: 10.1016/j.biortech.2017.12.004
Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17(1):10–2.
doi: 10.14806/ej.17.1.200
Zhang J, Kobert K, Flouri T, Stamatakis A. PEAR: a fast and accurate Illumina paired-end reAd mergeR. Bioinformatics. 2014;30(5):614–20.
pubmed: 24142950
doi: 10.1093/bioinformatics/btt593
Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics. 2011;27(6):863–4.
pubmed: 21278185
pmcid: 3051327
doi: 10.1093/bioinformatics/btr026
Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10(10):996–8.
pubmed: 23955772
doi: 10.1038/nmeth.2604
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb. 2009;75(23):7537–41.
doi: 10.1128/AEM.01541-09
Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013;31(9):814–21.
pubmed: 23975157
pmcid: 3819121
doi: 10.1038/nbt.2676
Tatusov RL, Koonin EV, Lipman DJ. A genomic perspective on protein families. Science. 1997;278(5338):631–7.
pubmed: 9381173
doi: 10.1126/science.278.5338.631
Louca S, Parfrey LW, Doebeli M. Decoupling function and taxonomy in the global ocean microbiome. Science. 2016;353(6305):1272–77.
pubmed: 27634532
doi: 10.1126/science.aaf4507
Tazi L, Breakwell DP, Harker AR, Crandall KA. Life in extreme environments: microbial diversity in Great Salt Lake. Utah Extremophiles. 2014;18(3):525–35.
pubmed: 24682608
doi: 10.1007/s00792-014-0637-x
Jacob JH, Hussein EI, Shakhatreh MAK, Cornelison CT. Microbial community analysis of the hypersaline water of the Dead Sea using high-throughput amplicon sequencing. MicrobiologyOpen. 2017;6(5):e00500.
pubmed: 28677326
pmcid: 5635157
doi: 10.1002/mbo3.500
Maldonado MJ, Albarracín VH, Lara JA, Ferrero MA, Farías ME. Culture-dependent and -independent methods reveal dominance of halophilic Euryarchaeota in high-altitude Andean lakes. Aquat Microb Ecol. 2018;81(2):171–88.
doi: 10.3354/ame01863
Torregrosa-Crespo J, Bergaust L, Pire C, Martínez-Espinosa RM. Denitrifying haloarchaea: sources and sinks of nitrogenous gases. FEMS Microbiol Lett. 2017;365(3):fnx270.
Alcántara-Hernández RJ, Cs V-E, Zavala-DÃaz, de la Serna FJ, Rodriguez-Revilla J, Dendooven L, Marsch R. Haloarchaeal assimilatory nitrate-reducing communities from a saline alkaline soil. FEMS Microbiol Lett. 2009; 298(1):56–66.
Jiang H, Huang J, Yang J. Halotolerant and halophilic microbes and their environmental implications in saline and hypersaline lakes in Qinghai Province, China. In: Extremophiles in eurasian ecosystems: ecology, diversity, and applications. vol. 8; 2018: 299–316.
Liu X, Li M, Castelle CJ, Probst AJ, Zhou Z, Pan J, Liu Y, Banfield JF, Gu J-D. Insights into the ecology, evolution, and metabolism of the widespread woesearchaeotal lineages. Microbiome. 2018;6(1):1–16.
doi: 10.1186/s40168-018-0488-2
Ortiz-Alvarez R, Casamayor EO. High occurrence of Pacearchaeota and Woesearchaeota (Archaea Superphylum DPANN) in the surface waters of oligotrophic high-altitude lakes. Environ Microbiol Rep. 2016;8(2):210–7.
pubmed: 26711582
doi: 10.1111/1758-2229.12370
Liu X, Wang Y, Gu JD. Ecological distribution and potential roles of Woesearchaeota in anaerobic biogeochemical cycling unveiled by genomic analysis. Comput Struct Biotechnol J. 2021;19:794–800.
pubmed: 33552450
pmcid: 7844129
doi: 10.1016/j.csbj.2021.01.013
Zhou J, Smith JA, Li M, Holmes DE. Methane production by Methanothrix thermoacetophila via direct interspecies electron transfer with Geobacter metallireducens. mBio. 2023;14(4):e0036023.
pubmed: 37306514
doi: 10.1128/mbio.00360-23
Vigderovich H, Eckert W, Elvert M, Gafni A, Rubin-Blum M, Bergman O, Sivan O. Aerobic methanotrophy increases the net iron reduction in methanogenic lake sediments. Front Microbiol. 2023;14:1206414.
pubmed: 37577416
pmcid: 10415106
doi: 10.3389/fmicb.2023.1206414
Gagliano MC, Sampara P, Plugge CM, Temmink H, Sudmalis D, Ziels RM, Atomi H. Functional insights of salinity stress-related pathways in metagenome-resolved Methanothrix genomes. Appl Environ Microb. 2022;88(10):e02449–21.
doi: 10.1128/aem.02449-21
Camacho A, Picazo A, Rochera C, Santamans A, Morant D, Miralles-Lorenzo J, Castillo-Escrivà A. Methane emissions in Spanish saline lakes: current rates, temperature and salinity responses, and evolution under different climate change scenarios. Water. 2017;9(9):659.
doi: 10.3390/w9090659
Parada AE, Fuhrman JA. Marine archaeal dynamics and interactions with the microbial community over 5 years from surface to seafloor. ISME J. 2017;11(11):2510–25.
pubmed: 28731479
pmcid: 5649162
doi: 10.1038/ismej.2017.104
Quan Z-X, Kim J-G, Gwak J-H, Jung M-Y, An S-U, Hyun J-H, Kang S, Rhee S-K. Distinct temporal dynamics of planktonic archaeal and bacterial assemblages in the bays of the Yellow Sea. PLoS ONE. 2019;14(8):e0221408.
doi: 10.1371/journal.pone.0221408
Yuan H, Zhang R, Li Q, Han Q, Lu Q, Wu J. Unveiling the ecological significance of phosphorus fractions in shaping bacterial and archaeal beta diversity in mesotrophic lakes. Front Microbiol. 2023;14:1279751.
pubmed: 37886062
pmcid: 10598868
doi: 10.3389/fmicb.2023.1279751
Zhang W, Chen R, Meng F, Yuan H, Geng M, Cheng L, Yin H, Xue B, Wang J. Ecosystem functioning is linked to microbial evenness and community composition along depth gradient in a semiarid lake. Ecol Indic. 2021; 132(2021):108314.
Weiss S, Van Treuren W, Lozupone C, Faust K, Friedman J, Deng Y, Xia LC, Xu ZZ, Ursell L, Alm EJ, et al. Correlation detection strategies in microbial data sets vary widely in sensitivity and precision. ISME J. 2016;10(7):1669–81.
pubmed: 26905627
pmcid: 4918442
doi: 10.1038/ismej.2015.235