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Abstract

Meromictic lakes usually harbour certain prevailing anoxygenic phototrophic bacteria in their anoxic zone, such as the purple sulfur bacterium (PSB) sp. LSW (hereafter LSW) in Lake Shunet, Siberia. PSBs have been suggested to play a vital role in carbon, nitrogen and sulfur cycling at the oxic–anoxic interface of stratified lakes; however, the ecological significance of PSBs in the lake remains poorly understood. In this study, we explored the potential ecological role of LSW using a deep-sequencing analysis of single-cell genomics associated with flow cytometry. An approximately 2.7 Mb draft genome was obtained based on the co-assembly of five single-cell genomes. LSW might grow photolithoautotrophically and could play putative roles not only as a carbon fixer and diazotroph, but also as a sulfate reducer/oxidizer in the lake. This study provides insights into the potential ecological role of sp. in meromictic lakes.

Funding
This study was supported by the:
  • Ministry of Science and Technology, Taiwan (Award MOST105-2923-B-001-001-MY3)
    • Principle Award Recipient: Sen-LinTang
  • Russian Foundation for Basic Research (Award 21-54-52001)
    • Principle Award Recipient: DenisYu Rogozin
  • Ministry of Science and Technology, Taiwan (Award NSC102-2923-B-001-004-MY3)
    • Principle Award Recipient: Sen-LinTang
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2021-12-03
2024-04-26
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References

  1. Lauro FM, DeMaere MZ, Yau S, Brown MV, Ng C et al. An integrative study of a meromictic lake ecosystem in Antarctica. ISME J 2011; 5:879–895 [View Article] [PubMed]
    [Google Scholar]
  2. Comeau AM, Harding T, Galand PE, Vincent WF, Lovejoy C. Vertical distribution of microbial communities in a perennially stratified Arctic lake with saline, anoxic bottom waters. Sci Rep 2012; 2:604 [View Article] [PubMed]
    [Google Scholar]
  3. Andrei A-Ş, Robeson MS 2nd, Baricz A, Coman C, Muntean V et al. Contrasting taxonomic stratification of microbial communities in two hypersaline meromictic lakes. ISME J 2015; 9:2642–2656 [View Article] [PubMed]
    [Google Scholar]
  4. Zimmermann M, Escrig S, Hübschmann T, Kirf MK, Brand A et al. Phenotypic heterogeneity in metabolic traits among single cells of a rare bacterial species in its natural environment quantified with a combination of flow cell sorting and NanoSIMS. Front Microbiol 2015; 6:243 [View Article] [PubMed]
    [Google Scholar]
  5. Nobu MK, Dodsworth JA, Murugapiran SK, Rinke C, Gies EA et al. Phylogeny and physiology of candidate phylum ‘Atribacteria’ (OP9/JS1) inferred from cultivation-independent genomics. ISME J 2015; 10:273–286 [View Article]
    [Google Scholar]
  6. Baatar B, Chiang P-W, Rogozin DY, Wu Y-T, Tseng C-H et al. Bacterial communities of three saline meromictic lakes in central Asia. PLoS One 2016; 11:e0150847 [View Article] [PubMed]
    [Google Scholar]
  7. Wu Y-T, Yang C-Y, Chiang P-W, Tseng C-H, Chiu H-H et al. Comprehensive insights into composition, metabolic potentials, and interactions among archaeal, bacterial, and viral assemblages in meromictic Lake Shunet in Siberia. Front Microbiol 2018; 9:1763 [View Article] [PubMed]
    [Google Scholar]
  8. Klepac-Ceraj V, Hayes CA, Gilhooly WP, Lyons TW, Kolter R et al. Microbial diversity under extreme euxinia: Mahoney Lake, Canada. Geobiology 2012; 10:223–235 [View Article] [PubMed]
    [Google Scholar]
  9. Danza F, Ravasi D, Storelli N, Roman S, Lüdin S et al. Bacterial diversity in the water column of meromictic Lake Cadagno and evidence for seasonal dynamics. PLoS One 2018; 13:e0209743 [View Article] [PubMed]
    [Google Scholar]
  10. Lunina ON, Savvichev AS, Babenko VV, Boldyreva DI, Kuznetsov BB et al. Seasonal variations in the structure of an anoxygenic phototrophic bacterial community from the meromictic Lake Trekhtsvetnoe (Kandalaksha Bay, White Sea). Microbiology 2019; 88:100–114 [View Article]
    [Google Scholar]
  11. Overmann J, Beatty JT, Hall KJ. Purple sulfur bacteria control the growth of aerobic heterotrophic bacterioplankton in a meromictic salt lake. Appl Environ Microbiol 1996; 62:3251–3258 [View Article]
    [Google Scholar]
  12. Imhoff JF. The chromatiaceae. In Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E. eds The Prokaryotes New York: Springer; 2006 pp 846–873 [View Article]
    [Google Scholar]
  13. Casamayor EO, García-Cantizano J, Pedrós-Alió C. Carbon dioxide fixation in the dark by photosynthetic bacteria in sulfide-rich stratified lakes with oxic-anoxic interfaces. Limnol Oceanogr 2008; 53:1193–1203 [View Article]
    [Google Scholar]
  14. Casamayor EO, Llirós M, Picazo A, Barberán A, Borrego CM et al. Contribution of deep dark fixation processes to overall CO2 incorporation and large vertical changes of microbial populations in stratified karstic lakes. Aquat Sci 2011; 74:61–75 [View Article]
    [Google Scholar]
  15. Berg JS, Pjevac P, Sommer T, Buckner CRT, Philippi M et al. Dark aerobic sulfide oxidation by anoxygenic phototrophs in anoxic waters. Environ Microbiol 2019; 21:1611–1626 [View Article] [PubMed]
    [Google Scholar]
  16. Pjevac P, Dyksma S, Goldhammer T, Mujakić I, Koblížek M et al. In situ abundance and carbon fixation activity of distinct anoxygenic phototrophs in the stratified seawater Lake Rogoznica. Environ Microbiol 2019; 21:3896–3908 [View Article] [PubMed]
    [Google Scholar]
  17. Savvichev AS, Kadnikov VV, Rusanov II, Beletsky AV, Krasnova ED et al. Microbial processes and microbial communities in the water column of the polar meromictic Lake Bol’shie Khruslomeny at the White Sea Coast. Front Microbiol 2020; 11:1945 [View Article] [PubMed]
    [Google Scholar]
  18. Chan Y-F, Chiang P-W, Tandon K, Rogozin D, Degermendzhi A et al. Spatiotemporal changes in the bacterial community of the meromictic Lake Uchum, Siberia. Microb Ecol 2021; 81:357–369 [View Article] [PubMed]
    [Google Scholar]
  19. Di Nezio F, Beney C, Roman S, Danza F, Buetti-Dinh A et al. Anoxygenic photo- and chemo-synthesis of phototrophic sulfur bacteria from an alpine meromictic lake. FEMS Microbiol Ecol 2021; 97:fiab010 [View Article]
    [Google Scholar]
  20. Rogozin DY, Zykov VV, Ivanova EA, Anufrieva TN, Barkhatov YV et al. Meromixis and seasonal dynamics of vertical structure of Lake Uchum (South Siberia). Contemp Probl Ecol 2018; 11:195–206 [View Article]
    [Google Scholar]
  21. Rogozin DY, Zykov VV, Degermendzhi AG. Ecology of purple sulfur bacteria in the highly stratified meromictic Lake Shunet (Siberia, Khakassia) in 2002–2009. Microbiology 2012; 81:727–735 [View Article]
    [Google Scholar]
  22. Kallistova AYu, Kevbrina MV, Pimenov NV, Rusanov II, Rogozin DYu et al. Sulfate reduction and methanogenesis in the Shira and Shunet meromictic lakes (Khakasia, Russia). Microbiology 2006; 75:720–726 [View Article]
    [Google Scholar]
  23. Lauro FM, DeMaere MZ, Yau S, Brown MV, Ng C et al. An integrative study of a meromictic lake ecosystem in Antarctica. ISME J 2011; 5:879–895 [View Article] [PubMed]
    [Google Scholar]
  24. Sommer T, Danza F, Berg J, Sengupta A, Constantinescu G et al. Bacteria-induced mixing in natural waters. Geophys Res Lett 2017; 44:9424–9432 [View Article]
    [Google Scholar]
  25. Caumette P, Guyoneaud R, Imhoff JF, Süling J, Gorlenko V. Thiocapsa marina sp. nov., a novel, okenone-containing, purple sulfur bacterium isolated from brackish coastal and marine environments. Int J Syst Evol Microbiol 2004; 54:1031–1036 [View Article]
    [Google Scholar]
  26. Guyoneaud R, Süling J, Petri R, Matheron R, Caumette P et al. Taxonomic rearrangements of the genera Thiocapsa and Amoebobacter on the basis of 16S rDNA sequence analyses, and description of Thiolamprovum gen. nov. Int J Syst Bacteriol 1998; 48:957–964 [View Article]
    [Google Scholar]
  27. Schott J, Griffin BM, Schink B. Anaerobic phototrophic nitrite oxidation by Thiocapsa sp. strain KS1 and Rhodopseudomonas sp. strain LQ17. Microbiology 2010; 156:2428–2437 [View Article] [PubMed]
    [Google Scholar]
  28. Lunina ON, Bryantseva IA, Akimov VN, Rusanov II, Rogozin DYu et al. Seasonal changes in the structure of the anoxygenic photosynthetic bacterial community in Lake Shunet, Khakassia. Microbiology 2007; 76:368–379 [View Article]
    [Google Scholar]
  29. Thrash JC. Towards culturing the microbe of your choice. Environ Microbiol Rep 2021; 13:36–41 [View Article] [PubMed]
    [Google Scholar]
  30. Marcy Y, Ouverney C, Bik EM, Lösekann T, Ivanova N et al. Dissecting biological “dark matter” with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth. Proc Natl Acad Sci USA 2007; 104:11889–11894 [View Article] [PubMed]
    [Google Scholar]
  31. Hemp J, Lücker S, Schott J, Pace LA, Johnson JE et al. Genomics of a phototrophic nitrite oxidizer: insights into the evolution of photosynthesis and nitrification. ISME J 2016; 10:2669–2678 [View Article] [PubMed]
    [Google Scholar]
  32. Kashtan N, Roggensack SE, Rodrigue S, Thompson JW, Biller SJ et al. Single-cell genomics reveals hundreds of coexisting subpopulations in wild prochlorococcus. Science 2014; 344:416–420 [View Article] [PubMed]
    [Google Scholar]
  33. Mason OU, Han J, Woyke T, Jansson JK. Single-cell genomics reveals features of a Colwellia species that was dominant during the deepwater horizon oil spill. Front Microbiol 2014; 5:332 [View Article] [PubMed]
    [Google Scholar]
  34. Stepanauskas R. Single cell genomics: an individual look at microbes. Curr Opin Microbiol 2012; 15:613–620 [View Article] [PubMed]
    [Google Scholar]
  35. Casamayor EO, Ferrera I, Cristina X, Borrego CM, Gasol JM. Flow cytometric identification and enumeration of photosynthetic sulfur bacteria and potential for ecophysiological studies at the single-cell level. Environ Microbiol 2007; 9:1969–1985 [View Article] [PubMed]
    [Google Scholar]
  36. Rogozin DY, Degermendzhy AG. Hydraulically-operated thin-layer sampler for sampling heterogeneous water columns. J Sib Fed Univ, Biol 2008; 1:111–117 [View Article]
    [Google Scholar]
  37. Siegl A, Kamke J, Hochmuth T, Piel J, Richter M et al. Single-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME J 2011; 5:61–70 [View Article] [PubMed]
    [Google Scholar]
  38. Hamp TJ, Jones WJ, Fodor AA. Effects of experimental choices and analysis noise on surveys of the “rare biosphere”. Appl Environ Microbiol 2009; 75:3263–3270 [View Article] [PubMed]
    [Google Scholar]
  39. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  40. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article]
    [Google Scholar]
  41. Lindgreen S. Adapter removal: easy cleaning of next-generation sequencing reads. BMC Res Notes 2012; 5:337 [View Article] [PubMed]
    [Google Scholar]
  42. Li D, Liu C-M, Luo R, Sadakane K, Lam T-W. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 2015; 31:1674–1676 [View Article] [PubMed]
    [Google Scholar]
  43. Alneberg J, Bjarnason BS, de Bruijn I, Schirmer M, Quick J et al. Binning metagenomic contigs by coverage and composition. Nat Methods 2014; 11:1144–1146 [View Article] [PubMed]
    [Google Scholar]
  44. 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; 25:1043–1055 [View Article] [PubMed]
    [Google Scholar]
  45. Seemann T. Barrnap 0.7: Rapid Ribosomal RNA Prediction 2013 https:// github.com/tseemann/barrnap
  46. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 2012; 40:D109–D114 [View Article] [PubMed]
    [Google Scholar]
  47. Nawrocki EP, Eddy SR. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 2013; 29:2933–2935 [View Article] [PubMed]
    [Google Scholar]
  48. Nawrocki EP. Annotating functional RNAs in genomes using Infernal. Methods Mol Biol 2014; 1097:163–197 [View Article] [PubMed]
    [Google Scholar]
  49. Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 2007; 56:564–577 [View Article]
    [Google Scholar]
  50. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-Tree: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
    [Google Scholar]
  51. Letunic I, Bork P. Interactive tree of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article] [PubMed]
    [Google Scholar]
  52. Wu Y-W. ezTree: an automated pipeline for identifying phylogenetic marker genes and inferring evolutionary relationships among uncultivated prokaryotic draft genomes. BMC Genomics 2018; 19:921 [View Article]
    [Google Scholar]
  53. Bogorov LV. The properties of Thiocapsa roseopersicina, strain BBS, isolated from an estuary of the White Sea. Mikrobiologiia 1974; 43:326–332 [PubMed]
    [Google Scholar]
  54. Asao M, Takaichi S, Madigan MT. Thiocapsa imhoffii, sp. nov., an alkaliphilic purple sulfur bacterium of the family Chromatiaceae from Soap Lake, Washington (USA. Arch Microbiol 2007; 188:665–675 [View Article] [PubMed]
    [Google Scholar]
  55. Lunina ON, Bryantseva IA, Akimov VN, Rusanov II, Barinova ES et al. Anoxygenic phototrophic bacterial community of Lake Shira (Khakassia). Microbiology 2007; 76:469–479 [View Article]
    [Google Scholar]
  56. Parks DH, Rinke C, Chuvochina M, Chaumeil P-A, Woodcroft BJ et al. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat Microbiol 2017; 2:1533–1542 [View Article] [PubMed]
    [Google Scholar]
  57. Pfennig N. Ecology of phototrophic purple and green sulfur bacteria. In Schlegel HG, Bowien B. eds Autotrophic Bacteria New York: Springer-Verlag; 1989 pp 97–116
    [Google Scholar]
  58. Pfennig N. Genus Chromatium. In Staley JT, Bryant MP, Pfennig N, Holt JC. eds Bergey’s Manual of Systematic Bacteriology, 1st. edn vol. 3 Baltimore, MD: Williams and Wilkins; 1989 pp 1639–1643
    [Google Scholar]
  59. Zehr JP, Jenkins BD, Short SM, Steward GF. Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 2003; 5:539–554 [View Article] [PubMed]
    [Google Scholar]
  60. Schmidt K. Biosynthesis of carotenoids. In Clayton RK, Sistrom WR. eds The Photosynthetic Bacteria New York: Plenum Press; 1978 pp 729–750
    [Google Scholar]
  61. Kovács ÁT, Rákhely G, Kovács KL. Genes involved in the biosynthesis of photosynthetic pigments in the purple sulfur photosynthetic bacterium Thiocapsa roseopersicina. Appl Environ Microbiol 2003; 69:3093–3102 [View Article]
    [Google Scholar]
  62. Olson JM, Stanton EK. Absorption and fluorescence spectra of bacterial chlorophylls in situ. In Vernon LP, Seely GR. eds The Chlorophylls New York: Academic Press; 1966 pp 381–398
    [Google Scholar]
  63. Baumgarth N, Bigos M. Optimization of emission optics for multicolor flow cytometry. Methods Cell Biol 2004; 75:3–22 [View Article] [PubMed]
    [Google Scholar]
  64. Kondratieva EN. Interrelation between modes of carbon assimilation and energy production in phototrophic purple and green bacteria. In Quale JR. ed Microbial Biochemistry: International Review of Biochemistry vol. 21 Baltimore, MD: University Park Press; 1979 pp 117–175
    [Google Scholar]
  65. Yeates TO, Kerfeld CA, Heinhorst S, Cannon GC, Shively JM. Protein-based organelles in bacteria: carboxysomes and related microcompartments. Nat Rev Microbiol 2008; 6:681–691 [View Article] [PubMed]
    [Google Scholar]
  66. Kimber MS. Carboxysomal carbonic anhydrases. In Frost SC, McKenna R. eds Carbonic Anhydrase: Mechanism, Regulation, Links to Disease, and Industrial Applications Dordrecht: Springer; 2014 pp 89–103
    [Google Scholar]
  67. Trüper HG. CO2-Fixierung und Intermediärstoffwechsel bei Chromatium okenii Perty. Archiv Mikrobiol 1964; 49:23–50 [View Article]
    [Google Scholar]
  68. Bonin P. Anaerobic nitrate reduction to ammonium in two strains isolated from coastal marine sediment: a dissimilatory pathway. FEMS Microbiol Ecol 1996; 19:27–38 [View Article]
    [Google Scholar]
  69. Trüper HG, Fischer U. Anaerobic oxidation of sulphur compounds as electron donors for bacterial photosynthesis. Phil Trans R Soc Lond B 1997; 298:529–542 [View Article]
    [Google Scholar]
  70. Brown CM, Herbert RA. Ammonia assimilation in purple and green sulphur bacteria. FEMS Microbiol Lett 1977; 1:39–42 [View Article]
    [Google Scholar]
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