1887

Abstract

The aerobic primarily chemoorganotrophic actinobacterial strain MWH-Mo1 was isolated from a freshwater lake and is characterized by small cell lengths of less than 1 µm, small cell volumes of 0.05–0.06 µm (ultramicrobacterium), a small genome size of 1.75 Mbp and, at least for an actinobacterium, a low DNA G+C content of 54.6 mol%. Phylogenetic analyses based on concatenated amino acid sequences of 116 housekeeping genes suggested the type strain of affiliated with the family as its closest described relative. Strain MWH-Mo1 shares with the type strain of that species a 16S rRNA gene sequence similarity of 99.6 % but the genomes of the two strains share an average nucleotide identity of only 79.3 %. Strain MWH-Mo1 is in many genomic, phenotypic and chemotaxonomic characteristics quite similar to the type strain of . Previous intensive investigations revealed two unusual traits of strain MWH-Mo1. Although the strain is not known to be phototrophic, the metabolism is adjusted to the diurnal light cycle by up- and down-regulation of genes in light and darkness. This results in faster growth in the presence of light. Additionally, a cell size-independent protection against predation by bacterivorous flagellates, most likely mediated by a proteinaceous cell surface structure, was demonstrated. For the previously intensively investigated aerobic chemoorganotrophic actinobacterial strain MWH-Mo1 (=CCUG 56426=DSM 107758), the establishment of the new species sp. nov. is proposed.

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2021-08-25
2024-05-01
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References

  1. Nakai R, Baba T, Niki H, Nishijima M, Naganuma T. Aurantimicrobium minutum gen. nov., sp. nov., a novel ultramicrobacterium of the family Microbacteriaceae, isolated from river water. Int J Syst Evol Microbiol 2015; 65:4072–4079 [View Article] [PubMed]
    [Google Scholar]
  2. Nakai R. Size matters: Ultra-small and filterable microorganisms in the environment. Microbes Environ 2020; 35: [View Article] [PubMed]
    [Google Scholar]
  3. Nakai R, Fujisawa T, Nakamura Y, Nishide H, Uchiyama I et al. Complete genome sequence of Aurantimicrobium minutum type strain KNCT, a planktonic ultramicrobacterium isolated from river water. Genome Announc 2016; 4:e00616 [View Article]
    [Google Scholar]
  4. 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]
  5. Tarao M, Jezbera J, Hahn MW. Involvement of cell surface structures in size-independent grazing resistance of freshwater Actinobacteria. Appl Environ Microbiol 2009; 75:4720–4726 [View Article] [PubMed]
    [Google Scholar]
  6. Hahn MW, Pöckl M. Ecotypes of planktonic Actinobacteria with identical 16S rRNA genes adapted to thermal niches in temperate, subtropical, and tropical freshwater habitats. Appl Environ Microbiol 2005; 71:766–773 [View Article] [PubMed]
    [Google Scholar]
  7. Sharma AK, Sommerfeld K, Bullerjahn GS, Matteson AR, Wilhelm SW et al. Actinorhodopsin genes discovered in diverse freshwater habitats and among cultivated freshwater Actinobacteria. ISME J 2009; 3:726–737 [View Article]
    [Google Scholar]
  8. Maresca JA, Keffer JL, Hempel PP, Polson SW, Shevchenko O et al. Light modulates the physiology of nonphototrophic Actinobacteria. J Bacteriol 2019; 201:e00740–00718 [View Article] [PubMed]
    [Google Scholar]
  9. Sasaki J, Uramoto M, Nakase T, Komagata K. Cryobacterium psychrophilum gen. nov., sp. nov., nom. rev., comb. nov., an obligately psychrophilic actinomycete to accommodate “Curtobacterium psychrophilum” Inoue and Komagata 1976. Int J Syst Evol Microbiol 1997; 47:474–478
    [Google Scholar]
  10. Dastager SG, Lee J-C, Ju Y-J, Park D-J, Kim C-J. Cryobacterium mesophilum sp. nov., a novel mesophilic bacterium. Int J Syst Evol Microbiol 2008; 58:1241–1244 [View Article] [PubMed]
    [Google Scholar]
  11. 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 Meth 2004; 57:379–390 [View Article] [PubMed]
    [Google Scholar]
  12. Sánchez-Clemente R, Igeño MI, Población AG, Guijo MI, Merchán F et al. Study of pH changes in media during bacterial growth of several environmental strains. Proc Int Conf Automot User Interfaces Interact Veh Appl (2014) 2018; 2:1297 [View Article]
    [Google Scholar]
  13. Pitt A, Schmidt J, Koll U, Hahn MW. Aquiluna borgnonia gen. nov., sp. nov., a member of a Microbacteriaceae lineage of freshwater bacteria with small genome sizes. Int J Syst Evol Microbiol 2021; 71:004825 [View Article]
    [Google Scholar]
  14. Nakai R, Shibuya E, Justel A, Rico E, Quesada A et al. Phylogeographic analysis of filterable bacteria with special reference to Rhizobiales strains that occur in cryospheric habitats. Antarct Sci 2013; 25:219–228 [View Article]
    [Google Scholar]
  15. Hahn MW, Schmidt J, Taipale SJ, Doolittle WF, Koll U. Rhodoluna lacicola gen. nov., sp. nov., a planktonic freshwater bacterium with stream-lined genome. Int J Syst Evol Microbiol 2014; 64:3254–3263 [View Article] [PubMed]
    [Google Scholar]
  16. Vieira S, Huber KJ, Neumann-Schaal M, Geppert A, Luckner M et al. Usitatibacter rugosus gen. nov., sp. nov. and Usitatibacter palustris sp. nov., novel members of Usitatibacteraceae fam. nov. within the order Nitrosomonadales isolated from soil. Int J Syst Evol Microbiol 2021; 71: [View Article] [PubMed]
    [Google Scholar]
  17. Schumann P, Kalensee F, Cao J, Criscuolo A, Clermont D et al. Reclassification of Haloactinobacterium glacieicola as Occultella glacieicola gen. nov., comb. nov., of Haloactinobacterium album as Ruania alba comb. nov, with an emended description of the genus Ruania, recognition that the genus names Haloactinobacterium and Ruania are heterotypic synonyms and description of Occultella aeris sp. nov., a halotolerant isolate from surface soil sampled at an ancient copper smelter. Int J Syst Evol Microbiol 2021; 71: [View Article]
    [Google Scholar]
  18. Schumann P. Peptidoglycan structure. Rainey F, Oren A. eds In Methods in Microbiology, Vol 38: Taxonomy of Prokaryotes 2011 pp 101–129
    [Google Scholar]
  19. 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]
  20. Chen IMA, Markowitz VM, Chu K, Palaniappan K, Szeto E et al. IMG/M: integrated genome and metagenome comparative data analysis system. Nucleic Acids Res 2017; 45:D516D507
    [Google Scholar]
  21. Pitt A, Schmidt J, Koll U, Hahn MW. Rhodoluna limnophila sp. nov., a bacterium with 1.4 Mbp genome size isolated from freshwater habitats located in Salzburg, Austria. Int J Syst Evol Microbiol 2019; 69:3946–3954 [View Article] [PubMed]
    [Google Scholar]
  22. Kang I, Lee K, Yang S-J, Choi A, Kang D et al. Genome sequence of “Candidatus Aquiluna” sp. strain IMCC13023, a marine member of the Actinobacteria isolated from an arctic fjord. J Bacteriol 2012; 194:3550–3551 [View Article] [PubMed]
    [Google Scholar]
  23. Cho BC, Hardies SC, Jang GI, Hwang CY. Complete genome of streamlined marine actinobacterium Pontimonas salivibrio strain CL-TW6T adapted to coastal planktonic lifestyle. BMC Genomics 2018; 19:625 [View Article] [PubMed]
    [Google Scholar]
  24. Xu L, Dong Z, Fang L, Luo Y, Wei Z et al. OrthoVenn2: a web server for whole-genome comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res 2019; 47:W52–W58 [View Article] [PubMed]
    [Google Scholar]
  25. Alikhan N-F, Petty NK, Ben Zakour NL, Beatson SA. blast Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 2011; 12:402 [View Article] [PubMed]
    [Google Scholar]
  26. Ravenhall M, Škunca N, Lassalle F, Dessimoz C. Inferring horizontal gene transfer. PLoS Comp Biol 2015; 11:e1004095 [View Article]
    [Google Scholar]
  27. Lu J, Salzberg SL. SKEWIT: The skew index test for large-scale GC skew analysis of bacterial genomes. PLoS Comp Biol 2020; 16:e1008439
    [Google Scholar]
  28. Pushkarev A, Inoue K, Larom S, Flores-Uribe J, Singh M et al. A distinct abundant group of microbial rhodopsins discovered using functional metagenomics. Nature 2018; 558:595–599 [View Article] [PubMed]
    [Google Scholar]
  29. Keffer JL, Hahn MW, Maresca JA. Characterization of an unconventional rhodopsin from the freshwater actinobacterium Rhodoluna lacicola. J Bacteriol 2015; 197:2704–2712 [View Article] [PubMed]
    [Google Scholar]
  30. 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]
  31. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. mega X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article]
    [Google Scholar]
  32. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial-DNA in humans and chimpanzees. Mol Biol Evol 1993; 10:512–526
    [Google Scholar]
  33. Katoh K, Kuma K, Toh H, Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 2005; 33:511–518 [View Article]
    [Google Scholar]
  34. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000; 17:540–552 [View Article]
    [Google Scholar]
  35. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article]
    [Google Scholar]
  36. Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for Inference of Large Phylogenetic Trees New Orleans, LA: IEEE; 2010
    [Google Scholar]
  37. Schumann P, Zhang D-C, Redzic M, Margesin R. Alpinimonas psychrophila gen. nov., sp. nov., an actinobacterium of the family Microbacteriaceae isolated from alpine glacier cryoconite. Int J Syst Evol Microbiol 2012; 62:2724–2730 [View Article] [PubMed]
    [Google Scholar]
  38. Rodriguez-R L, Konstantinidis K. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Preprints 2016
    [Google Scholar]
  39. Konstantinidis KT, Ramette A, Tiedje JM. The bacterial species definition in the genomic era. Phil Trans R Soc B 2006; 361:1929–1940 [View Article]
    [Google Scholar]
  40. Stackebrandt E, Ebers J. Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 2006; 33:152–155
    [Google Scholar]
  41. Jaspers E, Overmann J. Ecological significance of microdiversity: Identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies. Appl Environ Microbiol 2004; 70:4831–4839 [View Article] [PubMed]
    [Google Scholar]
  42. Pitt A, Koll U, Schmidt J, Hahn MW. Aquirufa ecclesiirivi sp. nov. and Aquirufa beregesia sp. nov., isolated from a small creek and classification of Allopseudarcicella aquatilis as a later heterotypic synonym of Aquirufa nivalisilvae. Int J Syst Evol Microbiol 2020; 70:4602–4609 [View Article] [PubMed]
    [Google Scholar]
  43. Hoetzinger M, Schmidt J, Pitt A, Koll U, Lang E et al. Polynucleobacter paneuropaeus sp. nov., characterized by six strains isolated from freshwater lakes located along a 3000 km north–south cross-section across Europe. Int J Syst Evol Microbiol 2019; 69:203–213 [View Article] [PubMed]
    [Google Scholar]
  44. Hahn MW, Jezberova J, Koll U, Saueressig-Beck T, Schmidt J. Complete ecological isolation and cryptic diversity in Polynucleobacter bacteria not resolved by 16S rRNA gene sequences. ISME J 2016; 10:1642–1655
    [Google Scholar]
  45. Hahn MW, Koll U, Schmidt J, Huymann LR, Karbon G et al. Polynucleobacter hirudinilacicola sp. nov. and Polynucleobacter campilacus sp. nov. both isolated from freshwater systems. Int J Syst Evol Microbiol 2018; 68:2593–2601 [View Article] [PubMed]
    [Google Scholar]
  46. Hahn MW, Huemer A, Pitt A, Hoetzinger M. Opening a next-generation black box: ecological trends for hundreds of species-like taxa uncovered within a single bacterial >99% 16S rRNA operational taxonomic unit. Mol Ecol Res 2021; 00:1–15
    [Google Scholar]
  47. Neuenschwander SM, Ghai R, Pernthaler J, Salcher MM. Microdiversification in genome-streamlined ubiquitous freshwater Actinobacteria. ISME J 2018; 12:185–198 [View Article] [PubMed]
    [Google Scholar]
  48. Kasalicky V, Jezbera J, Simek K, Hahn MW. Limnohabitans planktonicus sp. nov. and Limnohabitans parvus sp. nov., planktonic betaproteobacteria isolated from a freshwater reservoir, and emended description of the genus Limnohabitans. Int J Syst Evol Microbiol 2010; 60:2710–2714 [View Article] [PubMed]
    [Google Scholar]
  49. Pitt A, Schmidt J, Koll U, Hahn MW. Aquirufa antheringensis gen. nov., sp. nov. and Aquirufa nivalisilvae sp. nov., representing a new genus of widespread freshwater bacteria. Int J Syst Evol Microbiol 2019; 69:2739–2749 [View Article] [PubMed]
    [Google Scholar]
  50. Shibukawa A, Kojima K, Nakajima Y, Nishimura Y, Yoshizawa S et al. Photochemical characterization of a new heliorhodopsin from the Gram-negative Eubacterium Bellilinea caldifistulae (BcHeR) and comparison with heliorhodopsin-48C12. Biochemistry 2019; 58:2934–2943 [View Article] [PubMed]
    [Google Scholar]
  51. Nakajima Y, Kojima K, Kashiyama Y, Doi S, Nakai R et al. Bacterium lacking a known gene for retinal biosynthesis constructs functional rhodopsins. Microbes Environ 2020; 35:ME20085 [View Article]
    [Google Scholar]
  52. Hahn MW, Höfle MG. Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol Ecol 2001; 35:113–121 [View Article] [PubMed]
    [Google Scholar]
  53. Boenigk J, Stadler P, Wiedlroither A, Hahn MW. Strain-specific differences in the grazing sensitivities of closely related ultramicrobacteria affiliated with the Polynucleobacter cluster. Appl Environ Microbiol 2004; 70:5787–5793 [View Article] [PubMed]
    [Google Scholar]
  54. Watanabe K, Komatsu N, Ishii Y, Negishi M. Effective isolation of bacterioplankton genus Polynucleobacter from freshwater environments grown on photochemically degraded dissolved organic matter. FEMS Microbiol Ecol 2009; 67:57–68 [View Article] [PubMed]
    [Google Scholar]
  55. Watanabe K, Ishii Y, Komatsu N, Kitamura T, Watanabe M et al. Growth rates and tolerance to low water temperatures of freshwater bacterioplankton strains: ecological insights from shallow hypereutrophic lakes in Japan. Hydrobiologia 2017; 792:67–81 [View Article]
    [Google Scholar]
  56. Crump BC, Hobbie JE. Synchrony and seasonality of bacterioplankton communities in two temperate rivers. Limnol Oceanogr 2005; 50:1718–1729
    [Google Scholar]
  57. Balmonte JP, Arnosti C, Underwood S, McKee BA, Teske A. Riverine bacterial communities reveal environmental disturbance signatures within the Betaproteobacteria and Verrucomicrobia. Front Microbiol 2016; 7:1441
    [Google Scholar]
  58. Liu Z, Huang S, Sun G, Xu Z, Xu M. Phylogenetic diversity, composition and distribution of bacterioplankton community in the Dongjiang River, China. FEMS Microbiol Ecol 2012; 80:30–44 [View Article] [PubMed]
    [Google Scholar]
  59. Parte AC. LPSN – List of Prokaryotic names with Standing in Nomenclature (bacterio.net), 20 years on. Int J Syst Evol Microbiol 2018; 68:1825–1829 [View Article] [PubMed]
    [Google Scholar]
  60. Liu Q, Song W-Z, Zhou Y-G, Dong X-Z, Xin Y-H. Phenotypic divergence of thermotolerance: Molecular basis and cold adaptive evolution related to intrinsic DNA flexibility of glacier-inhabiting Cryobacterium strains. Environ Microbiol 2020; 22:1409–1420 [View Article] [PubMed]
    [Google Scholar]
  61. Bajerski F, Ganzert L, Mangelsdorf K, Lipski A, Wagner D. Cryobacterium arcticum sp. nov., a psychrotolerant bacterium from an Arctic soil. Int J Syst Evol Microbiol 2011; 61:1849–1853 [View Article] [PubMed]
    [Google Scholar]
  62. Liu Q, Xin Y-H, Chen X-L, Liu H-C, Zhou Y-G et al. Cryobacterium aureum sp. nov., a psychrophilic bacterium isolated from glacier ice collected from the ice tongue surface. Int J Syst Evol Microbiol 2018; 68:1173–1176 [View Article] [PubMed]
    [Google Scholar]
  63. Liu Q, Tian J-H, Liu H-C, Zhou Y-G, Xin Y-H. Cryobacterium ruanii sp. nov. and Cryobacterium breve sp. nov., isolated from glaciers. Int J Syst Evol Microbiol 2020; 70:1918–1923 [View Article] [PubMed]
    [Google Scholar]
  64. Liu Q, Liu H, Wen Y, Zhou Y, Xin Y. Cryobacterium flavum sp. nov. and Cryobacterium luteum sp. nov., isolated from glacier ice. Int J Syst Evol Microbiol 2012; 62:1296–1299 [View Article] [PubMed]
    [Google Scholar]
  65. Liu Q, Liu H, Zhang J, Zhou Y, Xin Y. Cryobacterium levicorallinum sp. nov., a psychrophilic bacterium isolated from glacier ice. Int J Syst Evol Microbiol 2013; 63:2819–2822 [View Article] [PubMed]
    [Google Scholar]
  66. Liu Q, Tian J-H, Liu H-C, Zhou Y-G, Xin Y-H. Cryobacterium melibiosiphilum sp. nov., a psychrophilic bacterium isolated from glacier ice. Int J Syst Evol Microbiol 2019; 69:3276–3280 [View Article] [PubMed]
    [Google Scholar]
  67. Reddy GSN, Pradhan S, Manorama R, Shivaji S. Cryobacterium roopkundense sp. nov., a psychrophilic bacterium isolated from glacial soil. Int J Syst Evol Microbiol 2010; 60:866–870 [View Article] [PubMed]
    [Google Scholar]
  68. Gong C, Lai Q, Cai H, Jiang Y, Liao H et al. Cryobacterium soli sp. nov., isolated from forest soil. Int J Syst Evol Microbiol 2020; 70:675–679 [View Article] [PubMed]
    [Google Scholar]
  69. Liu Q, Liu H-C, Zhou Y-G, Xin Y-H. Genetic diversity of glacier-inhabiting Cryobacterium bacteria in China and description of Cryobacterium zongtaii sp. nov. and Arthrobacter glacialis sp. nov. Syst Appl Microbiol 2019; 42:168–177 [View Article] [PubMed]
    [Google Scholar]
  70. Wang Y, Cao P, Sun P, Zhao J, Sun X et al. Cryobacterium tepidiphilum sp. nov., isolated from rhizosphere soil of lettuce (var. ramosa Hort. Antonie van Leeuwenhoek 2019; 112:1611–1621 [View Article] [PubMed]
    [Google Scholar]
  71. Li A-H, Liu H-C, Xin Y-H, Kim S-G, Zhou Y-G. Glaciihabitans tibetensis gen. nov., sp. nov., a psychrotolerant bacterium of the family Microbacteriaceae, isolated from glacier ice water. Int J Syst Evol Microbiol 2014; 64:579–587 [View Article] [PubMed]
    [Google Scholar]
  72. Tiago I, Pires C, Mendes V, Morais PV, da Costa M et al. Microcella putealis gen. nov., sp nov., a Gram-positive alkaliphilic bacterium isolated from a nonsaline alkaline groundwater. Syst Appl Microbiol 2005; 28:479–487 [View Article] [PubMed]
    [Google Scholar]
  73. Tiago I, Morais PV, da Costa MS, Veríssimo A. Microcella alkaliphila sp. nov., a novel member of the family Microbacteriaceae isolated from a non-saline alkaline groundwater, and emended description of the genus Microcella. Int J Syst Evol Microbiol 2006; 56:2313–2316 [View Article] [PubMed]
    [Google Scholar]
  74. Dahal RH, Kim J. Glaciihabitans arcticus sp. nov., a psychrotolerant bacterium isolated from Arctic soil. Int J Syst Evol Microbiol 2019; 69:2492–2497 [View Article] [PubMed]
    [Google Scholar]
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