1887

Abstract

The genus belongs to the family (order , phylum ) and harbours aerobic chemoheterotrophic bacteria. Members of this genus were isolated from various aquatic habitats, and our analysis based on global amplicon sequencing data revealed that their relative abundance can reach up to 5–10 % of the bacterioplankton in soda lakes and pans. Although a remarkable fraction of the most frequent genotypes that we identified from continental aquatic habitats is still uncultured, five new alkaliphilic strains were characterized in detail in this study, which were isolated from three different soda lakes and pans of the Carpathian Basin (Hungary). Cells of all strains were Gram-stain-negative, obligate aerobic, rod-shaped, non-motile and non-spore-forming. The isolates were oxidase- and catalase-positive, red-coloured, but did not contain flexirubin-type pigments; they formed bright red colonies that were circular, smooth and convex. Their major isoprenoid quinone was MK-7 and the predominant fatty acids were iso-C, iso-C 3-OH and summed feature 3 containing C 6 and/or C 7. The polar lipid profiles contained phosphatidylethanolamine, an unidentified aminophospholipid, an unidentified glycolipid, and several unidentified lipids and aminolipids. Based on whole-genome sequences, the DNA G+C content was 37.0, 37.1 and 37.8 mol % for strains R4-6, DMA-N-10a and U6F3, respectively. The distinction of three new species was confirmed by genomic comparison. Orthologous average nucleotide identity (<85.4 %) and digital DNA–DNA hybridization values (<38.9 %) supported phenotypic, chemotaxonomic and 16S rRNA gene sequence data and, therefore, the following three novel species are proposed: sp. nov. (represented by strains R4-6=DSM 111903=JCM 34281=UCCCB122 and S4-10), sp. nov. (DMA-N-10a=DSM 107340=JCM 34280=UCCCB121) and sp. nov. (U6F3=DSM 111904=JCM 34282=UCCCB123 and U6F1). Emended descriptions of species , , , and are also presented.

Funding
This study was supported by the:
  • Magyar Tudományos Akadémia (Award BO/00837/20/8)
    • Principle Award Recipient: TamasFelfoldi
  • Wenner-Gren Stiftelserna
    • Principle Award Recipient: AttilaSzabó
  • Biorecover Horizon2020 (Award 821096)
    • Principle Award Recipient: PaulaV. Morais
  • Fundação para a Ciência e a Tecnologia (Award UID/EMS/00285/2020)
    • Principle Award Recipient: PaulaV. Morais
  • National Research, Development and Innovation Office (Award FK 138789)
    • Principle Award Recipient: TamasFelfoldi
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.005928
2023-06-16
2024-04-27
Loading full text...

Full text loading...

References

  1. Cottrell MT, Kirchman DL. Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl Environ Microbiol 2000; 66:1692–1697 [View Article] [PubMed]
    [Google Scholar]
  2. Thomas F, Hehemann J-H, Rebuffet E, Czjzek M, Michel G. Environmental and gut Bacteroidetes: the food connection. Front Microbiol 2011; 2:93 [View Article] [PubMed]
    [Google Scholar]
  3. Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S. A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev 2011; 75:14–49 [View Article] [PubMed]
    [Google Scholar]
  4. Yilmaz P, Yarza P, Rapp JZ, Glöckner FO. Expanding the world of marine bacterial and archaeal clades. Front Microbiol 2015; 6:1524 [View Article] [PubMed]
    [Google Scholar]
  5. Szabó A, Korponai K, Somogyi B, Vajna B, Vörös L et al. Grazing pressure-induced shift in planktonic bacterial communities with the dominance of acIII-A1 actinobacterial lineage in soda pans. Sci Rep 2020; 10:19871 [View Article] [PubMed]
    [Google Scholar]
  6. Schagerl M. Soda Lakes of East Africa Cham: Springer; 2016 [View Article]
    [Google Scholar]
  7. Boros E, Kolpakova M. A review of the defining chemical properties of soda lakes and pans: an assessment on a large geographic scale of Eurasian inland saline surface waters. PLoS One 2018; 13:e0202205 [View Article] [PubMed]
    [Google Scholar]
  8. Kebede E, Mariam ZG, Ahlgren I. The Ethiopian rift valley lakes: chemical characteristics of a salinity-alkalinity series. Hydrobiologia 1994; 288:1–12 [View Article]
    [Google Scholar]
  9. Felföldi T. Microbial communities of soda lakes and pans in the Carpathian Basin: a review. Biol Futur 2020; 71:393–404 [View Article] [PubMed]
    [Google Scholar]
  10. Lanzén A, Simachew A, Gessesse A, Chmolowska D, Jonassen I et al. Surprising prokaryotic and eukaryotic diversity, community structure and biogeography of Ethiopian soda lakes. PLoS One 2013; 8:e72577 [View Article] [PubMed]
    [Google Scholar]
  11. Korponai K, Szabó A, Somogyi B, Boros E, Borsodi AK et al. Dual bloom of green algae and purple bacteria in an extremely shallow soda pan. Extremophiles 2019; 23:467–477 [View Article] [PubMed]
    [Google Scholar]
  12. Szabó A, Korponai K, Kerepesi C, Somogyi B, Vörös L et al. Soda pans of the Pannonian steppe harbor unique bacterial communities adapted to multiple extreme conditions. Extremophiles 2017; 21:639–649 [View Article] [PubMed]
    [Google Scholar]
  13. Szuróczki S, Szabó A, Korponai K, Felföldi T, Somogyi B et al. Prokaryotic community composition in a great shallow soda lake covered by large reed stands (Neusiedler See/Lake Fertő) as revealed by cultivation- and DNA-based analyses. FEMS Microbiol Ecol 2020; 96:fiaa159 [View Article] [PubMed]
    [Google Scholar]
  14. Antony CP, Kumaresan D, Hunger S, Drake HL, Murrell JC et al. Microbiology of Lonar lake and other soda lakes. ISME J 2013; 7:468–476 [View Article] [PubMed]
    [Google Scholar]
  15. Borsodi AK, Knáb M, Czeibert K, Márialigeti K, Vörös L et al. Planktonic bacterial community composition of an extremely shallow soda pond during a phytoplankton bloom revealed by cultivation and molecular cloning. Extremophiles 2013; 17:575–584 [View Article] [PubMed]
    [Google Scholar]
  16. Matyugina EB, Borzenko SV, Matafonov PV, Belkova NL. A laboratory experiment for meromixis in an integrated sample of soda lake Doroninskoye (Transbaikalia). Curr Res Microbiol Biotechnol 2014; 2:398–401
    [Google Scholar]
  17. Hahnke RL, Meier-Kolthoff JP, García-López M, Mukherjee S, Huntemann M et al. Genome-based taxonomic classification of Bacteroidetes. Front Microbiol 2016; 7:2003 [View Article] [PubMed]
    [Google Scholar]
  18. Brettar I, Christen R, Höfle MG. Aquiflexum balticum gen. nov., sp. nov., a novel marine bacterium of the Cytophaga-Flavobacterium-Bacteroides group isolated from surface water of the central Baltic Sea. Int J Syst Evol Microbiol 2004; 54:2335–2341 [View Article] [PubMed]
    [Google Scholar]
  19. Arun AB, Young C-C, Chen W-M, Hung M-H, Lai W-A et al. Belliella pelovolcani sp. nov., isolated from a mud-volcano in Taiwan. Int J Syst Evol Microbiol 2009; 59:2534–2537 [View Article] [PubMed]
    [Google Scholar]
  20. Akhwale JK, Göker M, Rohde M, Schumann P, Klenk H-P et al. Belliella kenyensis sp. nov., isolated from an alkaline lake. Int J Syst Evol Microbiol 2015; 65:457–462 [View Article] [PubMed]
    [Google Scholar]
  21. Zhong Z-P, Liu Y, Hou T-T, Zhou Y-G, Liu H-C et al. Belliella aquatica sp. nov., isolated from a saline lake. Int J Syst Evol Microbiol 2015; 65:1622–1627 [View Article] [PubMed]
    [Google Scholar]
  22. Song L, Liu H, Wang J, Huang Y, Dai X et al. Belliella marina sp. nov., isolated from seawater. Int J Syst Evol Microbiol 2015; 65:4353–4357 [View Article] [PubMed]
    [Google Scholar]
  23. Kozyreva L, Egorova D, Anan’ina L, Plotnikova E, Ariskina E et al. Belliella buryatensis sp. nov., isolated from alkaline lake water. Int J Syst Evol Microbiol 2016; 66:137–143 [View Article] [PubMed]
    [Google Scholar]
  24. Szabó A, Márton Zs, Boros E, Vad CsF, Barteneva N et al. A matter of salt: the effect of salinity and water ionic composition on bacterial community structure based on global data. ISME J (submitted)
    [Google Scholar]
  25. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2013; 41:D590–6 [View Article] [PubMed]
    [Google Scholar]
  26. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 2009; 75:7537–7541 [View Article] [PubMed]
    [Google Scholar]
  27. R Core Team A Language and Environment for Statistical Computing. R Foundation for Statistical Computing Vienna, Austria: 2017
    [Google Scholar]
  28. Banciu H, Sorokin DY, Galinski EA, Muyzer G, Kleerebezem R et al. Thialkalivibrio halophilus sp. nov., a novel obligately chemolithoautotrophic, facultatively alkaliphilic, and extremely salt-tolerant, sulfur-oxidizing bacterium from a hypersaline alkaline lake. Extremophiles 2004; 8:325–334 [View Article] [PubMed]
    [Google Scholar]
  29. Csitári B, Bedics A, Felföldi T, Boros E, Nagy H et al. Anion-type modulates the effect of salt stress on saline lake bacteria. Extremophiles 2022; 26:12 [View Article] [PubMed]
    [Google Scholar]
  30. Banciu HL, Muntyan MS. Adaptive strategies in the double-extremophilic prokaryotes inhabiting soda lakes. Curr Opin Microbiol 2015; 25:73–79 [View Article] [PubMed]
    [Google Scholar]
  31. Louca S, Mazel F, Doebeli M, Parfrey LW. A census-based estimate of Earth’s bacterial and archaeal diversity. PLoS Biol 2019; 17:e3000106 [View Article] [PubMed]
    [Google Scholar]
  32. Sutcliffe IC, Rosselló-Móra R, Trujillo ME. Addressing the sublime scale of the microbial world: reconciling an appreciation of microbial diversity with the need to describe species. New Microbes New Infect 2021; 43:100931 [View Article] [PubMed]
    [Google Scholar]
  33. Boros E, Horváth Z, Wolfram G, Vörös L. Salinity and ionic composition of the shallow astatic soda pans in the Carpathian Basin. Ann Limnol - Int J Lim 2014; 50:59–69 [View Article]
    [Google Scholar]
  34. Boros E, Katalin V-B, Vörös L, Horváth Z. Multiple extreme environmental conditions of intermittent soda pans in the Carpathian Basin (Central Europe). Limnologica 2017; 62:38–46 [View Article] [PubMed]
    [Google Scholar]
  35. Dinka M, Ágoston-Szabó E, Berczik Á, Kutrucz G. Influence of water level fluctuation on the spatial dynamic of the water chemistry at Lake Fertõ/Neusiedler See. Limnologica 2004; 34:48–56 [View Article]
    [Google Scholar]
  36. Hahn MW, Lünsdorf H, Wu Q, Schauer M, Höfle MG et al. Isolation of novel ultramicrobacteria classified as Actinobacteria from five freshwater habitats in Europe and Asia. Appl Environ Microbiol 2003; 69:1442–1451 [View Article] [PubMed]
    [Google Scholar]
  37. Hahn MW, Stadler P, Wu QL, Pöckl M. The filtration-acclimatization method for isolation of an important fraction of the not readily cultivable bacteria. J Microbiol Methods 2004; 57:379–390 [View Article] [PubMed]
    [Google Scholar]
  38. Claus D. A standardized gram staining procedure. World J Microbiol Biotechnol 1992; 8:451–452 [View Article] [PubMed]
    [Google Scholar]
  39. Heimbrook ME, Wang WL, Campbell G. Staining bacterial flagella easily. J Clin Microbiol 1989; 27:2612–2615 [View Article] [PubMed]
    [Google Scholar]
  40. Bernardet J-F, Nakagawa Y, Holmes B. Proposed minimal standards for describing new taxa of the family Flavobacteriaceae and emendation of the family. Int J Syst Evol Microbiol 2002; 52:1070 [View Article] [PubMed]
    [Google Scholar]
  41. Barrow GI, Feltham RKA. Cowan and Steel’s Manual for the Identification of Medical Bacteria Cambridge: Cambridge University Press; 2003
    [Google Scholar]
  42. Smibert RM, Krieg NR. Phenotypic characterization. In Gerhardt P, Murray RGE, Wood WA, Krieg NR. eds Methods for General and Molecular Bacteriology Washington, DC: American Society for Microbiology; 1994 pp 603–711
    [Google Scholar]
  43. da Costa MS, Nobre MF, Wait R. Analysis of Lipids from Extremophilic Bacteria. In Rainey FA, Oren A. eds Methods in Microbiology vol 35 London: Academic Press; 2006 pp 127–159
    [Google Scholar]
  44. da Costa MS, Albuquerque L, Nobre MF, Wait R. The extraction and identification of respiratory lipoquinones of prokaryotes and their use in taxonomy. In Rainey F, Oren A. eds Methods in Microbiology vol 38 London: Academic Press; 2011 pp 197–206
    [Google Scholar]
  45. Morais PV, Francisco R, Branco R, Chung AP, da Costa MS. Leucobacter chromiireducens sp. nov, and Leucobacter aridicollis sp. nov., two new species isolated from a chromium contaminated environment. Syst Appl Microbiol 2004; 27:646–652 [View Article] [PubMed]
    [Google Scholar]
  46. da Costa MS, Albuquerque L, Nobre MF, Wait R. The identification of fatty acids in bacteria. In Rainey F, Oren A. eds Methods in Microbiology vol 38 London: Academic Press; 2011 pp 183–196
    [Google Scholar]
  47. Kirchman DL. The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol Ecol 2002; 39:91–100 [View Article] [PubMed]
    [Google Scholar]
  48. Buchan A, LeCleir GR, Gulvik CA, González JM. Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol 2014; 12:686–698 [View Article] [PubMed]
    [Google Scholar]
  49. Máthé I, Borsodi AK, Tóth EM, Felföldi T, Jurecska L et al. Vertical physico-chemical gradients with distinct microbial communities in the hypersaline and heliothermal lake Ursu (Sovata, Romania). Extremophiles 2014; 18:501–514 [View Article] [PubMed]
    [Google Scholar]
  50. Felföldi T, Fikó RD, Mentes A, Kovács E, Máthé I et al. Quisquiliibacterium transsilvanicum gen. nov., sp. nov., a novel betaproteobacterium isolated from a waste-treating bioreactor. Int J Syst Evol Microbiol 2017; 67:4742–4746 [View Article] [PubMed]
    [Google Scholar]
  51. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [View Article] [PubMed]
    [Google Scholar]
  52. Pruesse E, Peplies J, Glöckner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012; 28:1823–1829 [View Article] [PubMed]
    [Google Scholar]
  53. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article] [PubMed]
    [Google Scholar]
  54. Kim M, Oh HS, Park SC, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article] [PubMed]
    [Google Scholar]
  55. Felföldi T, Szabó A, Tóth E, Schumann P, Kéki Z et al. Sapientia aquatica gen. nov., sp. nov., isolated from a crater lake. Int J Syst Evol Microbiol 2020; 70:346–351 [View Article] [PubMed]
    [Google Scholar]
  56. Lee I, Ouk Kim Y, Park S-C, Chun J. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016; 66:1100–1103 [View Article] [PubMed]
    [Google Scholar]
  57. Kim D, Park S, Chun J. Introducing EzAAI: a pipeline for high throughput calculations of prokaryotic average amino acid identity. J Microbiol 2021; 59:476–480 [View Article] [PubMed]
    [Google Scholar]
  58. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinf 2013; 14:1–14 [View Article] [PubMed]
    [Google Scholar]
  59. Meier-Kolthoff JP, Klenk H-P, Göker M. Taxonomic use of DNA G+C content and DNA-DNA hybridization in the genomic age. Int J Syst Evol Microbiol 2014; 64:352–356 [View Article] [PubMed]
    [Google Scholar]
  60. Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M. TYGS and LPSN: a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res 2022; 50:D801–D807 [View Article] [PubMed]
    [Google Scholar]
  61. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 2018; 36:996–1004 [View Article] [PubMed]
    [Google Scholar]
  62. Parks DH, Chuvochina M, Chaumeil P-A, Rinke C, Mussig AJ et al. A complete domain-to-species taxonomy for Bacteria and Archaea. Nat Biotechnol 2020; 38:1079–1086 [View Article] [PubMed]
    [Google Scholar]
  63. Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH, Hancock J. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 2019; 36:1925–1927 [View Article] [PubMed]
    [Google Scholar]
  64. Matsen FA, Kodner RB, Armbrust EV. pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinf 2010; 11:538 [View Article] [PubMed]
    [Google Scholar]
  65. Konstantinidis KT, Rosselló-Móra R, Amann R. Uncultivated microbes in need of their own taxonomy. ISME J 2017; 11:2399–2406 [View Article] [PubMed]
    [Google Scholar]
  66. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article] [PubMed]
    [Google Scholar]
  67. Mukherjee S, Seshadri R, Varghese NJ, Eloe-Fadrosh EA, Meier-Kolthoff JP et al. 1,003 reference genomes of bacterial and archaeal isolates expand coverage of the tree of life. Nat Biotechnol 2017; 35:676–683 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.005928
Loading
/content/journal/ijsem/10.1099/ijsem.0.005928
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error