Microbial assemblages and associated biogeochemical processes in Lake Bonney, a permanently ice-covered lake in the McMurdo Dry Valleys, Antarctica.
Biogeochemical cycles
Cryosphere
Hypersaline
Metagenomics
Microbial metabolism
Journal
Environmental microbiome
ISSN: 2524-6372
Titre abrégé: Environ Microbiome
Pays: England
ID NLM: 101768168
Informations de publication
Date de publication:
20 Aug 2024
20 Aug 2024
Historique:
received:
29
04
2024
accepted:
13
08
2024
medline:
20
8
2024
pubmed:
20
8
2024
entrez:
19
8
2024
Statut:
epublish
Résumé
Lake Bonney, which is divided into a west lobe (WLB) and an east lobe (ELB), is a perennially ice-covered lake located in the McMurdo Dry Valleys of Antarctica. Despite previous reports on the microbial community dynamics of ice-covered lakes in this region, there is a paucity of information on the relationship between microbial genomic diversity and associated nutrient cycling. Here, we applied gene- and genome-centric approaches to investigate the microbial ecology and reconstruct microbial metabolic potential along the depth gradient in Lake Bonney. Lake Bonney is strongly chemically stratified with three distinct redox zones, yielding different microbial niches. Our genome enabled approach revealed that in the sunlit and relatively freshwater epilimnion, oxygenic photosynthetic production by the cyanobacterium Pseudanabaena and a diversity of protists and microalgae may provide new organic carbon to the environment. CO-oxidizing bacteria, such as Acidimicrobiales, Nanopelagicales, and Burkholderiaceae were also prominent in the epilimnion and their ability to oxidize carbon monoxide to carbon dioxide may serve as a supplementary energy conservation strategy. In the more saline metalimnion of ELB, an accumulation of inorganic nitrogen and phosphorus supports photosynthesis despite relatively low light levels. Conversely, in WLB the release of organic rich subglacial discharge from Taylor Glacier into WLB would be implicated in the possible high abundance of heterotrophs supported by increased potential for glycolysis, beta-oxidation, and glycoside hydrolase and may contribute to the growth of iron reducers in the dark and extremely saline hypolimnion of WLB. The suboxic and subzero temperature zones beneath the metalimnia in both lobes supported microorganisms capable of utilizing reduced nitrogens and sulfurs as electron donors. Heterotrophs, including nitrate reducing sulfur oxidizing bacteria, such as Acidimicrobiales (MAG72) and Salinisphaeraceae (MAG109), and denitrifying bacteria, such as Gracilimonas (MAG7), Acidimicrobiales (MAG72) and Salinisphaeraceae (MAG109), dominated the hypolimnion of WLB, whereas the environmental harshness of the hypolimnion of ELB was supported by the relatively low in metabolic potential, as well as the abundance of halophile Halomonas and endospore-forming Virgibacillus. The vertical distribution of microbially driven C, N and S cycling genes/pathways in Lake Bonney reveals the importance of geochemical gradients to microbial diversity and biogeochemical cycles with the vertical water column.
Sections du résumé
BACKGROUND
BACKGROUND
Lake Bonney, which is divided into a west lobe (WLB) and an east lobe (ELB), is a perennially ice-covered lake located in the McMurdo Dry Valleys of Antarctica. Despite previous reports on the microbial community dynamics of ice-covered lakes in this region, there is a paucity of information on the relationship between microbial genomic diversity and associated nutrient cycling. Here, we applied gene- and genome-centric approaches to investigate the microbial ecology and reconstruct microbial metabolic potential along the depth gradient in Lake Bonney.
RESULTS
RESULTS
Lake Bonney is strongly chemically stratified with three distinct redox zones, yielding different microbial niches. Our genome enabled approach revealed that in the sunlit and relatively freshwater epilimnion, oxygenic photosynthetic production by the cyanobacterium Pseudanabaena and a diversity of protists and microalgae may provide new organic carbon to the environment. CO-oxidizing bacteria, such as Acidimicrobiales, Nanopelagicales, and Burkholderiaceae were also prominent in the epilimnion and their ability to oxidize carbon monoxide to carbon dioxide may serve as a supplementary energy conservation strategy. In the more saline metalimnion of ELB, an accumulation of inorganic nitrogen and phosphorus supports photosynthesis despite relatively low light levels. Conversely, in WLB the release of organic rich subglacial discharge from Taylor Glacier into WLB would be implicated in the possible high abundance of heterotrophs supported by increased potential for glycolysis, beta-oxidation, and glycoside hydrolase and may contribute to the growth of iron reducers in the dark and extremely saline hypolimnion of WLB. The suboxic and subzero temperature zones beneath the metalimnia in both lobes supported microorganisms capable of utilizing reduced nitrogens and sulfurs as electron donors. Heterotrophs, including nitrate reducing sulfur oxidizing bacteria, such as Acidimicrobiales (MAG72) and Salinisphaeraceae (MAG109), and denitrifying bacteria, such as Gracilimonas (MAG7), Acidimicrobiales (MAG72) and Salinisphaeraceae (MAG109), dominated the hypolimnion of WLB, whereas the environmental harshness of the hypolimnion of ELB was supported by the relatively low in metabolic potential, as well as the abundance of halophile Halomonas and endospore-forming Virgibacillus.
CONCLUSIONS
CONCLUSIONS
The vertical distribution of microbially driven C, N and S cycling genes/pathways in Lake Bonney reveals the importance of geochemical gradients to microbial diversity and biogeochemical cycles with the vertical water column.
Identifiants
pubmed: 39160591
doi: 10.1186/s40793-024-00605-1
pii: 10.1186/s40793-024-00605-1
doi:
Types de publication
Journal Article
Langues
eng
Pagination
60Subventions
Organisme : Korea Polar Research Institute
ID : PE23130
Organisme : Korea Polar Research Institute
ID : PE23130
Organisme : Korea Polar Research Institute
ID : PE23130
Organisme : Korea Polar Research Institute
ID : PE23130
Organisme : Korea Polar Research Institute
ID : PE23130
Organisme : Korea Polar Research Institute
ID : PE23130
Organisme : Korea Polar Research Institute
ID : PE23130
Organisme : National Science Foundation
ID : OPP 1637708
Organisme : National Science Foundation
ID : OPP 1637708
Informations de copyright
© 2024. The Author(s).
Références
Guo B, Li W, Santibáñez P, Priscu JC, Liu Y, Liu K. Organic matter distribution in the icy environments of Taylor Valley. Antarctica Sci Total Environ. 2022;841: 156639.
pubmed: 35697215
Obryk MK, Doran PT, Fountain AG, Myers M, McKay CP. Climate from the McMurdo Dry Valleys, Antarctica, 1986–2017: surface air temperature trends and redefined summer season. J Geophys Res Atmos. 2020;125:e2019JD032180.
Priscu JC, Wolf CF, Takacs CD, Fritsen CH, Laybourn-Parry J, Roberts EC, et al. Carbon transformations in a perennially ice-covered Antarctic lake. Bioscience. 1999;49:997–1008.
Obryk MK, Doran PT, Priscu JC. The permanent ice cover of Lake Bonney, Antarctica: the influence of thickness and sediment distribution on photosynthetically available radiation and chlorophyll-a distribution in the underlying water column. J Geophys Res-Biogeosci. 2014;119:1879–91.
Fritsen CH, Priscu JC. Seasonal change in the optical properties of the permanent ice cover on Lake Bonney, Antarctica: consequences for lake productivity and phytoplankton dynamics. Limnol Oceanogr. 1999;44:447–54.
Spigel RH, Priscu JC, Obryk MK, Stone W, Doran PT. The physical limnology of a permanently ice-covered and chemically stratified Antarctic lake using high resolution spatial data from an autonomous underwater vehicle. Limnol Oceanogr. 2018;63:1234–52.
Gooseff MN, Barrett JE, Adams BJ, Doran PT, Fountain AG, Lyons WB, et al. Decadal ecosystem response to an anomalous melt season in a polar desert in Antarctica. Nat Ecol Evol. 2017;1:1334–8.
pubmed: 29046542
Spigel RH, Priscu JC. Physical limnology of the McMurdo Dry Valleys lakes. In: Priscu JC, editor. Ecosystem dynamics in a polar desert: the McMurdo Dry Valleys, Antarctica. Washington: American Geophysical Union; 1998. p. 153–87.
Sherwell S, Kalra I, Li W, McKnight DM, Priscu JC, Morgan-Kiss RM. Antarctic lake phytoplankton and bacteria from near-surface waters exhibit high sensitivity to climate-driven disturbance. Environ Microbiol. 2022;24:6017–32.
pubmed: 35860854
pmcid: 10084183
Kwon M, Kim M, Takacs-Vesbach C, Lee J, Hong SG, Kim SJ, et al. Niche specialization of bacteria in permanently ice-covered lakes of the McMurdo Dry Valleys. Antarctica Environ Microbiol. 2017;19:2258–71.
pubmed: 28276129
Rojas-Jimenez K, Wurzbacher C, Bourne EC, Chiuchiolo A, Priscu JC, Grossart H-P. Early diverging lineages within Cryptomycota and Chytridiomycota dominate the fungal communities in ice-covered lakes of the McMurdo Dry Valleys. Antarctica Sci Rep. 2017;7:15348.
pubmed: 29127335
Vick-Majors TJ, Priscu JC, Amaral-Zettler AL. Modular community structure suggests metabolic plasticity during the transition to polar night in ice-covered Antarctic lakes. ISME J. 2014;8:778–89.
pubmed: 24152712
Mikucki JA, Priscu JC. Bacterial diversity associated with blood falls, a subglacial outflow from the Taylor Glacier. Antarctica Appl Environ Microbiol. 2007;73:4029–39.
pubmed: 17468282
Lawrence JP, Doran PT, Winslow LA, Priscu JC. Subglacial brine flow and wind-induced internal waves in Lake Bonney. Antarctica Antarct Sci. 2020;32:223–37.
Badgeley JA, Pettit EC, Carr CG, Tulaczyk S, Mikucki JA, Lyons WB, Team MS. An englacial hydrologic system of brine within a cold glacier: Blood Falls, McMurdo Dry Valleys. Antarctica J Glaciol. 2017;63:387–400.
Priscu JC. Phytoplankton nutrient deficiency in lakes of the McMurdo dry valleys. Antarctica Freshw Biol. 1995;34:215–27.
Dore JE, Priscu JC. Phytoplankton phosphorus deficiency and alkaline phosphatase activity in the McMurdo Dry Valley lakes. Antarctica Limnol Oceanogr. 2001;46:1331–46.
Vick TJ, Priscu JC. Bacterioplankton productivity in lakes of the Taylor Valley, Antarctica, during the polar night transition. Aquat Microb Ecol. 2012;68:77–90.
Lee PA, Priscu JC, DiTullio GR, Riseman SF, Tursich N, de Mora SJ. Elevated levels of dimethylated-sulfur compounds in Lake Bonney, a poorly ventilated Antarctic lake. Limnol Oceanogr. 2004;49:1044–55.
Priscu JC. The biogeochemistry of nitrous oxide in permanently ice-covered lakes of the McMurdo Dry Valleys. Antarctica Glob Change Biol. 1997;3:301–15.
Priscu JC, Christner BC, Dore JE, Westley MB, Popp BN, Casciotti KL, Lyons WB. Supersaturated N
Ward BB, Granger J, Maldonado MT, Casciotti KL, Harris S, Wells ML. Denitrification in the hypolimnion of permanently ice-covered Lake Bonney. Antarctica Aquatic Microbial Ecology. 2005;38:295–307.
Lee PA, Mikucki JA, Foreman CM, Priscu JC, DiTullio GR, Riseman SF, et al. Thermodynamic constraints on microbially mediated processes in lakes of the McMurdo Dry Valleys. Antarctica Geomicrobiol J. 2004;21:221–37.
Li W, Morgan-Kiss RM. Influence of environmental drivers and potential interactions on the distribution of microbial communities from three permanently stratified Antarctic lakes. Front Microbiol. 2019;10:1067.
pubmed: 31156585
pmcid: 6530420
Bowman JS, Vick-Majors TJ, Morgan-Kiss R, Takacs-Vesbach C, Ducklow HW, Priscu JC. Microbial community dynamics in two polar extremes: the lakes of the McMurdo Dry Valleys and the West Antarctic Peninsula marine ecosystem. Bioscience. 2016;66:829–47.
Takacs-Vesbach C, Zeglin L, Barrett JE, Gooseff MN, Priscu JC, Doran P, Lyons WB. Factors promoting microbial diversity in the McMurdo Dry Valleys, Antarctica. In: Doran PT, Lyons WB, McKnight DM, editors. Life in Antarctic Deserts and other cold dry environments: astrobiological Analogs. Cambridge: Cambridge University Press; 2010. p. 221.
Takacs CD, Priscu JC, McKnight DM. Bacterial dissolved organic carbon demand in McMurdo Dry Valley lakes. Antarctica Limnol Oceanogr. 2001;46:1189–94.
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.
pubmed: 24695404
pmcid: 4103590
Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25:1754–60.
pubmed: 19451168
pmcid: 2705234
Li D, Luo R, Liu C-M, Leung C-M, Ting H-F, Sadakane K, et al. MEGAHIT v1. 0: a fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods. 2016;102:3–11.
pubmed: 27012178
Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 2010;11:1–11.
Mao X, Cai T, Olyarchuk JG, Wei L. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics. 2005;21:3787–93.
pubmed: 15817693
Rawlings ND, Barrett AJ, Bateman A. MEROPS: the peptidase database. Nucleic Acids Res. 2010;38:D227–33.
pubmed: 19892822
Garber AI, Nealson KH, Okamoto A, McAllister SM, Chan CS, Barco RA, Merino N. FeGenie: a comprehensive tool for the identification of iron genes and iron gene neighborhoods in genome and metagenome assemblies. Front Microbiol. 2020;11: 499513.
Tully BJ, Wheat CG, Glazer BT, Huber JA. A dynamic microbial community with high functional redundancy inhabits the cold, oxic subseafloor aquifer. ISME J. 2018;12:1–16.
pubmed: 29099490
Dahl C, Engels S, Pott-Sperling AS, Schulte A, Sander J, Lübbe Y, et al. Novel genes of the dsr gene cluster and evidence for close interaction of Dsr proteins during sulfur oxidation in the phototrophic sulfur bacterium Allochromatium vinosum. J Bacteriol. 2005;187:1392–404.
pubmed: 15687204
pmcid: 545617
Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:4673–80.
pubmed: 7984417
pmcid: 308517
Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–3.
pubmed: 24451623
pmcid: 3998144
Darriba D, Posada D, Kozlov AM, Stamatakis A, Morel B, Flouri T. ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Mol Biol Evol. 2020;37:291–4.
pubmed: 31432070
Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–9.
pubmed: 22388286
pmcid: 3322381
Alneberg J, Sundh J, Bennke C, Beier S, Lundin D, Hugerth LW, et al. BARM and BalticMicrobeDB, a reference metagenome and interface to meta-omic data for the Baltic Sea. Sci Data. 2018;5: 180146.
pubmed: 30063227
pmcid: 6067050
Wu YW, Simmons BA, Singer SW. MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics. 2016;32:605–7.
pubmed: 26515820
Kang DD, Li F, Kirton E, Thomas A, Egan R, An H, Wang Z. MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ. 2019;7: e7359.
pubmed: 31388474
pmcid: 6662567
Alneberg J, Bjarnason BS, De Bruijn I, Schirmer M, Quick J, Ijaz UZ, et al. Binning metagenomic contigs by coverage and composition. Nat Methods. 2014;11:1144–6.
pubmed: 25218180
Sieber CM, Probst AJ, Sharrar A, Thomas BC, Hess M, Tringe SG, Banfield JF. Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy. Nat Microbiol. 2018;3:836–43.
pubmed: 29807988
pmcid: 6786971
Olm MR, Brown CT, Brooks B, Banfield JF. dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J. 2017;11:2864–8.
pubmed: 28742071
pmcid: 5702732
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.
pubmed: 25977477
pmcid: 4484387
Bowers RM, Kyrpides NC, Stepanauskas R, Harmon-Smith M, Doud D, Reddy TBK, et al. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat Biotechnol. 2017;35:725–31.
pubmed: 28787424
pmcid: 6436528
Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Oxford: Oxford University Press; 2020.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547.
pubmed: 29722887
pmcid: 5967553
Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49:W293–6.
pubmed: 33885785
pmcid: 8265157
Graham E, Heidelberg J, Tully B. Potential for primary productivity in a globally-distributed bacterial phototroph. ISME J. 2018;12:1861–6.
pubmed: 29523891
pmcid: 6018677
Lizotte MP, Priscu JC. Photosynthesis irradiance relationships in phytoplankton from the physically stable water column of a perennially ice-covered lake (Lake Bonney, Antarctica). J Phycol. 1992;28:179–85.
Dolhi JM, Teufel AG, Kong WD, Morgan-Kiss RM. Diversity and spatial distribution of autotrophic communities within and between ice-covered Antarctic lakes (McMurdo Dry Valleys). Limnol Oceanogr. 2015;60:977–91.
Bayliss P, Ellis-Evans JC, Laybourn-Parry J. Temporal patterns of primary production in a large ultra-oligotrophic Antarctic freshwater lake. Polar Biol. 1997;18:363–70.
Morgan-Kiss R, Lizotte M, Kong W, Priscu J. Photoadaptation to the polar night by phytoplankton in a permanently ice-covered Antarctic lake. Limnol Oceanogr. 2016;61:3–13.
Patriarche JD, Priscu JC, Takacs-Vesbach C, Winslow L, Myers KF, Buelow H, et al. Year-round and long-term phytoplankton dynamics in Lake Bonney, a permanently ice-covered Antarctic Lake. J Geophys Res-Biogeosciences. 2021;126:e202JG005925.
Paerl HW, Priscu JC. Microbial phototrophic, heterotrophic, and diazotrophic activities associated with aggregates in the permanent ice cover of Lake Bonney. Antarctica Microbial Ecology. 1998;36:221–30.
pubmed: 9852502
Wing K, Priscu J. Microbial communities in the permanent ice cap of Lake Bonney, Antarctica: relationships among chlorophyll a, gravel and nutrients. Antarct J US. 1993;28:246–9.
King GM, Weber CF. Distribution, diversity and ecology of aerobic CO-oxidizing bacteria. Nat Rev Microbiol. 2007;5:107–18.
pubmed: 17224920
Meyer O, Fiebig K. Enzymes oxidizing carbon monoxide. In: Degn H, Cox RP, Toftlund H, editors. Gas enzymology. Dordrecht: Springer; 1985. p. 147–68.
Greening C, Grinter R. Microbial oxidation of atmospheric trace gases. Nat Rev Microbiol. 2022;20:513–28.
pubmed: 35414013
Lauro FM, DeMaere MZ, Yau S, Brown MV, Ng C, Wilkins D, et al. An integrative study of a meromictic lake ecosystem in Antarctica. ISME J. 2011;5:879–95.
pubmed: 21124488
Leach TH, Beisner BE, Carey CC, Pernica P, Rose KC, Huot Y, et al. Patterns and drivers of deep chlorophyll maxima structure in 100 lakes: the relative importance of light and thermal stratification. Limnol Oceanogr. 2018;63:628–46.
Morgan-Kiss RM, Priscu JC, Pocock T, Gudynaite-Savitch L, Huner NP. Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiol Mol Biol Rev. 2006;70:222–52.
pubmed: 16524924
pmcid: 1393254
Mikucki JA, Foreman CM, Sattler B, Berry Lyons W, Priscu JC. Geomicrobiology of Blood Falls: an iron-rich saline discharge at the terminus of the Taylor Glacier. Antarctica Aquat Geochem. 2004;10:199–220.
Joulak I, Finore I, Nicolaus B, Leone L, Moriello AS, Attia H, et al. Evaluation of the production of exopolysaccharides by newly isolated Halomonas strains from Tunisian hypersaline environments. Int J Biol Macromol. 2019;138:658–66.
pubmed: 31344416
Peng S, Kai M, Yang X, Luo Y, Bai L. Study on the osmoregulation of “Halomonas socia” NY-011 and the degradation of organic pollutants in the saline environment. Extremophiles. 2020;24:843–61.
pubmed: 32930883
Gray DA, Dugar G, Gamba P, Strahl H, Jonker MJ, Hamoen LW. Extreme slow growth as alternative strategy to survive deep starvation in bacteria. Nat Commun. 2019;10:890.
pubmed: 30792386
pmcid: 6385201
Priscu JC, Vincent WF, Howard-Williams C. Inorganic nitrogen uptake and regeneration in perennially icecovered Lakes Fryxell and Vanda. Antarctica J Plankton Res. 1989;11:335–51.
Priscu JC. Phytoplankton nutrient deficiency in lakes of the McMurdo dry valleys. Antarctica Freshwater Biol. 1995;34:215–27.
Voytek MA, Priscu JC, Ward BB. The distribution and relative abundance of ammonia-oxidizing bacteria in lakes of the McMurdo Dry Valley. Antarctica Hydrobiol. 1999;401:113–30.
Voytek MA, Ward BB, Priscu JC. The abundance of ammonium-oxidizing bacteria in Lake Bonney, Antarctica determined by immunofluorescence, Pcr and in situ hybridization. In: Priscu JC, editor. Ecosystem dynamics in a polar desert: the Mcmurdo Dry Valleys, Antarctica. Washington: American Geophysical Union; 1998. p. 217–28.
Gooseff MN, Barrett JE, Adams BJ, Doran PT, Fountain AG, Lyons WB, et al. Decadal ecosystem response to an anomalous melt season in a polar desert in Antarctica. Nat Ecol Evolution. 2017;1:1334–8.
Ward BB, Priscu JC. Detection and characterization of denitrifying bacteria from a permanently ice-covered Antarctic lake. Hydrobiologia. 1997;347:57–68.
Wadham JL, De’Ath R, Monteiro F, Tranter M, Ridgwell A, Raiswell R, Tulaczyk S. The potential role of the Antarctic Ice Sheet in global biogeochemical cycles. Earth Environ Sci Trans R Soc Edinb. 2013;104:55–67.
Gill-Olivas B, Telling J, Tranter M, Skidmore M, Christner B, O’Doherty S, Priscu J. Subglacial erosion has the potential to sustain microbial processes in Subglacial Lake Whillans. Antarctica Commun Earth Environ. 2021;2:134.