SALINITY-Induced Changes in Diversity, Stability, and Functional Profiles of Microbial Communities in Different Saline Lakes in Arid Areas.
Community assembly
Ecological functions
Extremophilic microorganisms
Microbial diversity
Saline lakes
Journal
Microbial ecology
ISSN: 1432-184X
Titre abrégé: Microb Ecol
Pays: United States
ID NLM: 7500663
Informations de publication
Date de publication:
01 Nov 2024
01 Nov 2024
Historique:
received:
19
04
2024
accepted:
02
10
2024
medline:
1
11
2024
pubmed:
1
11
2024
entrez:
1
11
2024
Statut:
epublish
Résumé
Saline lakes, characterized by high salinity and limited nutrient availability, provide an ideal environment for studying extreme halophiles and their biogeochemical processes. The present study examined prokaryotic microbial communities and their ecological functions in lentic sediments (with the salinity gradient and time series) using 16S rRNA amplicon sequencing and a metagenomic approach. Our findings revealed a negative correlation between microbial diversity and salinity. The notable predominance of Archaea in high-salinity lakes signified a considerable alteration in the composition of the microbial community. The results indicate that elevated salinity promotes homogeneous selection pressures, causing substantial alterations in microbial diversity and community structure, and simultaneously hindering interactions among microorganisms. This results in a notable decrease in the complexity of microbial ecological networks, ultimately influencing the overall ecological functional responses of microbial communities such as carbon fixation, sulfur, and nitrogen metabolism. Overall, our findings reveal salinity drives a notable predominance of Archaea, selects for species adapted to extreme conditions, and decreases microbial community complexity within saline lake ecosystems.
Identifiants
pubmed: 39482450
doi: 10.1007/s00248-024-02442-8
pii: 10.1007/s00248-024-02442-8
doi:
Substances chimiques
RNA, Ribosomal, 16S
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
135Subventions
Organisme : National Science and Technology Fundamental Resources Investigation Program of China
ID : 2021FY100900
Organisme : Natural Science Foundation of Xinjiang Uygur Autonomous Region
ID : 2022D01A154
Organisme : Key-Area Research and Development Programof Guangdong Province
ID : 2022B0202110001
Informations de copyright
© 2024. The Author(s).
Références
Armstrong A (2010) Lake carbon. Nat Geosci 3:151–151
doi: 10.1038/ngeo816
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477
pubmed: 22506599
pmcid: 3342519
doi: 10.1089/cmb.2012.0021
Baxter B, Eddington B, Riddle M, Webster T, Avery B (2007) Great Salt Lake halophilic microorganisms as models for astrobiology: evidence for desiccation tolerance and ultraviolet irradiation resistance. Vol 6694: SPIE
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857
pubmed: 31341288
pmcid: 7015180
doi: 10.1038/s41587-019-0209-9
Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12:59–60
pubmed: 25402007
doi: 10.1038/nmeth.3176
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP (2016) DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583
pubmed: 27214047
pmcid: 4927377
doi: 10.1038/nmeth.3869
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ et al (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108(Suppl 1):4516–4522
pubmed: 20534432
doi: 10.1073/pnas.1000080107
Chase JM, Myers JA (2011) Disentangling the importance of ecological niches from stochastic processes across scales. Philos Trans R Soc B: Biol Sci 366:2351–2363
doi: 10.1098/rstb.2011.0063
Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH (2022) GTDB-Tk v2: memory friendly classification with the genome taxonomy database. Bioinformatics 38:5315–5316
pubmed: 36218463
pmcid: 9710552
doi: 10.1093/bioinformatics/btac672
Chen H, Ma K, Huang Y, Yang Y, Ma Z, Chu C (2021) Salinity drives functional and taxonomic diversities in global water metagenomes. Front Microbiol 12:719725
pubmed: 34790175
pmcid: 8591284
doi: 10.3389/fmicb.2021.719725
Chen S (2023) Ultrafast one-pass FASTQ data preprocessing, quality control, and deduplication using fastp. iMeta 2:e107
pubmed: 38868435
pmcid: 10989850
doi: 10.1002/imt2.107
Csárdi G, Nepusz T (2006) The igraph software package for complex network research. InterJournal Complex Syst 1695(5):1–9
DasSarma S (2006) Extreme Halophiles are models for astrobiology. Microbe Mag 1:120–126
Ding X, Liu K, Gong G, Tian L, Ma J (2020) Volatile organic compounds in the salt-lake sediments of the Tibet Plateau influence prokaryotic diversity and community assembly. Extremophiles 24:307–318
pubmed: 32025854
doi: 10.1007/s00792-020-01155-3
Duarte CM, Prairie YT, Montes C, Cole JJ, Striegl R, Melack J, et al (2008) CO2 emissions from saline lakes: a global estimate of a surprisingly large flux. J Geophys Res: Biogeosci 113. https://doi.org/10.1029/2007JG000637
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376
pubmed: 7288891
doi: 10.1007/BF01734359
Fierer N, Leff JW, Adams BJ, Nielsen UN, Bates ST, Lauber CL et al (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc Natl Acad Sci 109:21390–21395
pubmed: 23236140
pmcid: 3535587
doi: 10.1073/pnas.1215210110
Geng K, Hu C (1989) Evolution trend of Jilantai Salt Lake. Journal of Beijing Normal University(Natural Science), pp 86–91
Ghori NU, Wise MJ, Whiteley AS (2021) Temporal microbial community dynamics within a unique acid saline lake. Front Microbiol 12:649594
pubmed: 34248867
pmcid: 8264302
doi: 10.3389/fmicb.2021.649594
Guan TW, Lin YJ, Ou MY, Chen KB (2020) Isolation and diversity of sediment bacteria in the hypersaline aiding lake. China PLoS One 15:e0236006
pubmed: 32649724
doi: 10.1371/journal.pone.0236006
Han J, Gao QX, Zhang YG, Li L, Mohamad OAA, Rao MPN, Xiao M, Hozzein WN, Alkhalifah DHM, Tao Y, Li WJ (2018) Transcriptomic and Ectoine Analysis of Halotolerant Nocardiopsis gilva YIM 90087(T) Under Salt Stress. Front Microbiol 9:618. https://doi.org/10.3389/fmicb.2018.00618
doi: 10.3389/fmicb.2018.00618
pubmed: 29651284
pmcid: 5884947
Han R, Zhang X, Liu J, Long Q, Chen L, Liu D et al (2017) Microbial community structure and diversity within hypersaline Keke Salt Lake environments. Can J Microbiol 63:895–908
pubmed: 28850799
doi: 10.1139/cjm-2016-0773
He Y, He L, Wang Z, Liang T, Sun S, Liu X (2022) Salinity shapes the microbial communities in surface sediments of salt lakes on the Tibetan Plateau. China Water 14:4043
doi: 10.3390/w14244043
Huang J, Yang J, Jiang H, Wu G, Liu W, Wang B, Xiao H, Han J (2020) Microbial Responses to Simulated Salinization and Desalinization in the Sediments of the Qinghai-Tibetan Lakes. Front Microbiol 11:1772. https://doi.org/10.3389/fmicb.2020.01772
doi: 10.3389/fmicb.2020.01772
pubmed: 32849396
pmcid: 7426462
Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119
pubmed: 20211023
pmcid: 2848648
doi: 10.1186/1471-2105-11-119
Jiang H, Dong H, Yu B, Liu X, Li Y, Ji S et al (2007) Microbial response to salinity change in Lake Chaka, a hypersaline lake on Tibetan plateau. Environ Microbiol 9:2603–2621
pubmed: 17803783
doi: 10.1111/j.1462-2920.2007.01377.x
Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30
pubmed: 10592173
pmcid: 102409
doi: 10.1093/nar/28.1.27
Kang DD, Li F, Kirton E, Thomas A, Egan R, An H et al (2019) MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ 7:e7359
pubmed: 31388474
doi: 10.7717/peerj.7359
Li X, Liu Q, Yu X, Zhang C, Liu M, Zhou X et al (2022) Spatial pattern and co-occurrence network of microbial community in response to extreme environment of salt lakes on the Qinghai-Tibet Plateau. Environ Sci Pollut Res 30(8):20615–20630
doi: 10.1007/s11356-022-23572-x
Liu M, Liu XX, He XL, Liu LJ, Wu H, Tang CX, Zhang YS, Jin CW (2017) Ethylene and nitric oxide interact to regulate the magnesium deficiency-induced root hair development in Arabidopsis. New Phytol 213:1242–1256. https://doi.org/10.1111/nph.14259
doi: 10.1111/nph.14259
pubmed: 27775153
Liu Q, Yang J, Wang B, Liu W, Hua Z, Jiang H (2022) Influence of salinity on the diversity and composition of carbohydrate metabolism, nitrogen and sulfur cycling genes in lake surface sediments. Front Microbiol 13:1019010
pubmed: 36519167
pmcid: 9742235
doi: 10.3389/fmicb.2022.1019010
Louca S, Parfrey LW, Doebeli M (2016) Decoupling function and taxonomy in the global ocean microbiome. Science 353:1272–1277
pubmed: 27634532
doi: 10.1126/science.aaf4507
Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet 17:10
doi: 10.14806/ej.17.1.200
Matthew RO, Christopher TB, Brandon B, Jillian FB (2017) dRep: a tool for fast and accurate genome de-replication that enables tracking of microbial genotypes and improved genome recovery from metagenomes. bioRxiv 108142. https://doi.org/10.1101/108142
McMurdie PJ, Holmes S (2012) Phyloseq: a bioconductor package for handling and analysis of high-throughput phylogenetic sequence data. Pac Symp Biocomput 235–46. https://doi.org/10.1142/9789814366496_0023
Oren A (2011) Thermodynamic limits to microbial life at high salt concentrations. Environ Microbiol 13:1908–1923
pubmed: 21054738
doi: 10.1111/j.1462-2920.2010.02365.x
Oyewusi HA, Abdul Wahab R, Edbeib MF, Mohamad MAN, Abdul Hamid AA, Kaya Y et al (2021) Functional profiling of bacterial communities in Lake Tuz using 16S rRNA gene sequences. Biotechnol Biotechnol Equip 35:1–10
doi: 10.1080/13102818.2020.1840437
Oyewusi HA, Wahab RA, Kaya Y, Edbeib MF, Huyop F (2020) Alternative bioremediation agents against haloacids, haloacetates and chlorpyrifos using novel halogen-degrading bacterial isolates from the hypersaline Lake Tuz. Catalysts 10:651
doi: 10.3390/catal10060651
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25:1043–1055
pubmed: 25977477
doi: 10.1101/gr.186072.114
Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124
pubmed: 25061070
pmcid: 4609014
doi: 10.1093/bioinformatics/btu494
Post FJ (1977) The microbial ecology of the Great Salt Lake. Microb Ecol 3:143–165
pubmed: 24233467
doi: 10.1007/BF02010403
Price MN, Dehal PS, Arkin AP (2010) FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490
pubmed: 20224823
pmcid: 2835736
doi: 10.1371/journal.pone.0009490
Reed HE, Martiny JBH (2013) Microbial composition affects the functioning of estuarine sediments. ISME J 7:868–879
pubmed: 23235294
doi: 10.1038/ismej.2012.154
Saini A, Kumar A, Singh G, Giri SK (2023) Survival strategies and stress adaptations in halophilic archaebacteria. Microbial Stress Response: Mechanisms and Data Science. American Chemical Society, pp. 1–21
Santini TC, Gramenz L, Southam G, Zammit C (2022) Microbial community structure is most strongly associated with geographical distance and pH in salt lake sediments. Front Microbiol 13:920056
pubmed: 35756015
pmcid: 9221066
doi: 10.3389/fmicb.2022.920056
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS et al (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60
pubmed: 21702898
pmcid: 3218848
doi: 10.1186/gb-2011-12-6-r60
Shu W-S, Huang L-N (2022) Microbial diversity in extreme environments. Nat Rev Microbiol 20:219–235
pubmed: 34754082
doi: 10.1038/s41579-021-00648-y
Shurigin V, Hakobyan A, Panosyan H, Egamberdieva D, Davranov K, Birkeland NK (2019) A glimpse of the prokaryotic diversity of the Large Aral Sea reveals novel extremophilic bacterial and archaeal groups. Microbiologyopen 8:e00850
pubmed: 31058468
pmcid: 6741134
doi: 10.1002/mbo3.850
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
pubmed: 25156418
pmcid: 4158274
doi: 10.1007/s00792-014-0670-9
Tazi L, Breakwell DP, Harker AR, Crandall KA (2014) Life in extreme environments: microbial diversity in Great Salt Lake. Utah Extremophiles 18:525–535
pubmed: 24682608
doi: 10.1007/s00792-014-0637-x
Tranvik LJ, Downing JA, Cotner JB, Loiselle SA, Striegl RG, Ballatore TJ et al (2009) Lakes and reservoirs as regulators of carbon cycling and climate. Limnol Oceanogr 54:2298–2314
doi: 10.4319/lo.2009.54.6_part_2.2298
Wang B, Huang J, Yang J, Jiang H, Xiao H, Han J, Zhang X (2021) Bicarbonate uptake rates and diversity of RuBisCO genes in saline lake sediments. FEMS Microbiol Ecol 97(4):37
doi: 10.1093/femsec/fiab037
Wang CF, Han GL, Yang ZR, Li Y-X, Wang BS (2022) Plant Salinity Sensors: Current Understanding and Future Directions. Frontiers in Plant Science 13. https://doi.org/10.3389/fpls.2022.859224
Wang L, Lian C, Wan W, Qiu Z, Luo X, Huang Q et al (2023) Salinity-triggered homogeneous selection constrains the microbial function and stability in lakes. Appl Microbiol Biotechnol 107:6591–6605
pubmed: 37688597
doi: 10.1007/s00253-023-12696-w
Weinisch L, Kühner S, Roth R, Grimm M, Roth T, Netz DJA, Pierik AJ, Filker S (2018) Identification of osmoadaptive strategies in the halophile, heterotrophic ciliate Schmidingerothrix salinarum. PLOS Biology 16:e2003892. https://doi.org/10.1371/journal.pbio.2003892
doi: 10.1371/journal.pbio.2003892
pubmed: 29357351
pmcid: 5794333
Woolway RI, Kraemer BM, Lenters JD, Merchant CJ, O’Reilly CM, Sharma S (2020) Global lake responses to climate change. Nat Rev Earth Environ 1:388–403
doi: 10.1038/s43017-020-0067-5
Wurtsbaugh WA, Miller C, Null SE, DeRose RJ, Wilcock P, Hahnenberger M et al (2017) Decline of the world’s saline lakes. Nat Geosci 10:816–821
doi: 10.1038/ngeo3052
Xie YG, Luo ZH, Fang BZ, Jiao JY, Xie QJ, Cao XR et al (2022) Functional differentiation determines the molecular basis of the symbiotic lifestyle of Ca. Nanohaloarchaeota Microbiome 10:172
pubmed: 36242054
doi: 10.1186/s40168-022-01376-y
Yang J, Han M, Zhao Z, Han J, Zhang X, Xie Z, Jiang H (2022) Microbial response to multiple-level addition of grass organic matter in lake sediments with different salinity. FEMS Microbiol Ecol 98(4):fiac046
pubmed: 35425979
doi: 10.1093/femsec/fiac046
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
pubmed: 31165352
doi: 10.1007/s11427-018-9525-9
Yang J, Jiang H, Liu W, Huang L, Huang J, Wang B et al (2020) Potential utilization of terrestrially derived dissolved organic matter by aquatic microbial communities in saline lakes. Isme j 14:2313–2324
pubmed: 32483305
pmcid: 7608266
doi: 10.1038/s41396-020-0689-0
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
doi: 10.1080/01490451.2017.1382611
Yang J, La Ma, 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
pubmed: 27113678
pmcid: 4844989
doi: 10.1038/srep25078
Yue L, Kong W, Ji M, Liu J, Morgan-Kiss RM (2019) Community response of microbial primary producers to salinity is primarily driven by nutrients in lakes. Sci Total Environ 696:134001
pubmed: 31454602
doi: 10.1016/j.scitotenv.2019.134001
Zaikova E, Benison KC, Mormile MR, Johnson SS (2018) Microbial communities and their predicted metabolic functions in a desiccating acid salt lake. Extremophiles 22:367–379
pubmed: 29350297
doi: 10.1007/s00792-018-1000-4
Zhang L, Tan X, Zhang X (2012) Analysis on the status, countermeasures to development and utilization. J Salt Chem Ind 41:7–10+18
Zhang Y, Wu G, Jiang H, Yang J, She W, Khan I, Li W (2018) Abundant and rare microbial biospheres respond differently to environmental and spatial factors in Tibetan hot springs. Front Microbiol 9:2096
pubmed: 30283408
pmcid: 6156277
doi: 10.3389/fmicb.2018.02096
Zhao Y, Liu P, Rui J, Cheng L, Wang Q, Liu X et al (2020) Dark carbon fixation and chemolithotrophic microbial community in surface sediments of the cascade reservoirs, Southwest China. Sci Total Environ 698:134316
pubmed: 31783464
doi: 10.1016/j.scitotenv.2019.134316