1887

Abstract

The unusual chemo-organoheterotrophic proteobacterial strain MWH-Nonnen-W8red was isolated from a lake located in the Black Forest (Schwarzwald), Germany, by using the filtration-acclimatization method. Phylogenetic analyses based on the 16S rRNA gene sequence of the strain could not provide clear hints on classification of the strain in one of the current classes of the phylum Proteobacteria . Whole-genome sequencing resulted in a genome size of 3.5 Mbp and revealed a quite low DNA G+C content of 32.6 mol%. In-depth phylogenetic analyses based on alignments of 74 protein sequences of a phylogenetically broad range of taxa suggested assignment of the strain to a new order of the class Oligoflexia . These analyses also suggested that the order Bdellovibrionales should be transferred from the class Deltaproteobacteria to the class Oligoflexia , that this order should be split into two orders, and that the family Pseudobacteriovoracaceae should be transferred from the order Bdellovibrionales to the order Oligoflexales . We propose to establish for strain MWH-Nonnen-W8red (=DSM 23856=CCUG 58639) the novel species and genus Silvanigrella aquatica gen. nov., sp. nov. to be placed in the new family Silvanigrellaceae fam. nov. of the new order Silvanigrellales ord. nov.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.001965
2017-08-04
2019-10-21
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/67/8/2555.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.001965&mimeType=html&fmt=ahah

References

  1. Metchnikoff E. Contributions á l'etude du pleomorphisme des bacteriens.. Annales De l'Institut Pasteur 1889;3:61–68
    [Google Scholar]
  2. Rodrigues JL, Duffy MA, Tessier AJ, Ebert D, Mouton L et al. Phylogenetic characterization and prevalence of "Spirobacillus cienkowskii," a red-pigmented, spiral-shaped bacterial pathogen of freshwater Daphnia species. Appl Environ Microbiol 2008;74:1575–1582 [CrossRef][PubMed]
    [Google Scholar]
  3. Walke JB, Becker MH, Hughey MC, Swartwout MC, Jensen RV et al. Most of the dominant members of amphibian skin bacterial communities can be readily cultured. Appl Environ Microbiol 2015;81:6589–6600 [CrossRef][PubMed]
    [Google Scholar]
  4. Kip N, Fritz C, Langelaan ES, Pan Y, Bodrossy L et al. Methanotrophic activity and diversity in different Sphagnum magellanicum dominated habitats in the southernmost peat bogs of Patagonia. Biogeosciences 2012;9:47–55 [CrossRef]
    [Google Scholar]
  5. Shabarova T, Widmer F, Pernthaler J. Mass effects meet species sorting: transformations of microbial assemblages in epiphreatic subsurface karst water pools. Environ Microbiol 2013;15:2476–2488 [CrossRef][PubMed]
    [Google Scholar]
  6. Clingenpeel S, Macur RE, Kan J, Inskeep WP, Lovalvo D et al. Yellowstone Lake: high-energy geochemistry and rich bacterial diversity. Environ Microbiol 2011;13:2172–2185 [CrossRef][PubMed]
    [Google Scholar]
  7. Nakai R, Nishijima M, Tazato N, Handa Y, Karray F et al. Oligoflexus tunisiensis gen. nov., sp. nov., a Gram-negative, aerobic, filamentous bacterium of a novel proteobacterial lineage, and description of Oligoflexaceae fam. nov., Oligoflexales ord. nov. and Oligoflexia classis nov. Int J Syst Evol Microbiol 2014;64:3353–3359 [CrossRef][PubMed]
    [Google Scholar]
  8. 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 [CrossRef][PubMed]
    [Google Scholar]
  9. Reasoner DJ, Geldreich EE. A new medium for the enumeration and subculture of bacteria from potable water. Appl Environ Microbiol 1985;49:1–7[PubMed]
    [Google Scholar]
  10. Nakai R, Naganuma T. Oligoflexia, the newest class of the phylum Proteobacteria, consisting of only one cultured species and uncultured bacterial phylotypes from diverse habitats. J Phylogenetics Evol Biol 2015;3:141
    [Google Scholar]
  11. Marbach A, Shilo M. Dependence of marine bdellovibrios on potassium, calcium, and magnesium ions. Appl Environ Microbiol 1978;36:169–177[PubMed]
    [Google Scholar]
  12. Hahn MW, Lang E, Brandt U, Wu QL, Scheuerl T. Emended description of the genus Polynucleobacter and the species Polynucleobacter necessarius and proposal of two subspecies, P. necessarius subsp. necessarius subsp. nov.and P. necessariussubsp. asymbioticussubsp. nov. Int J Syst Evol Microbiol 2009;59:2002–2009 [CrossRef][PubMed]
    [Google Scholar]
  13. Hahn MW, Schmidt J, Pitt A, Taipale SJ, Lang E. Reclassification of four Polynucleobacter necessarius strains as representatives of Polynucleobacter asymbioticus comb. nov., Polynucleobacter duraquae sp. nov., Polynucleobacter yangtzensis sp. nov. and Polynucleobacter sinensis sp. nov., and emended description of Polynucleobacter necessarius. Int J Syst Evol Microbiol 2016;66:2883–2892 [CrossRef][PubMed]
    [Google Scholar]
  14. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsl 1990;20:16
    [Google Scholar]
  15. Tindall BJ. Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol Lett 1990;66:199–202 [CrossRef]
    [Google Scholar]
  16. Tindall BJ. A comparative study of the lipid composition of Halobacterium saccharovorum from various sources. Syst Appl Microbiol 1990;13:128–130 [CrossRef]
    [Google Scholar]
  17. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959;37:911–917 [CrossRef][PubMed]
    [Google Scholar]
  18. Schumann P. Peptidoglycan structure. In Rainey F, Oren A. (editors) Taxonomy of Prokaryotes. Methods in Microbiologyvol. 38 London: Academic Press; 2011; pp.101–129[CrossRef]
    [Google Scholar]
  19. Meincke L, Copeland A, Lapidus A, Lucas S, Berry KW et al. Complete genome sequence of Polynucleobacter necessarius subsp. asymbioticus type strain (QLW-P1DMWA-1T). Stand Genomic Sci 2012;6:74–83 [CrossRef][PubMed]
    [Google Scholar]
  20. Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E et al. IMG: the integrated microbial genomes database and comparative analysis system. Nucleic Acids Res 2012;40:D115–D122 [CrossRef][PubMed]
    [Google Scholar]
  21. Chen H, Brinkac LM, Mishra P, Li N, Lymperopoulou DS et al. Draft genome sequences for the obligate bacterial predators Bacteriovorax spp. of four phylogenetic clusters. Stand Genomic Sci 2015;10:11 [CrossRef][PubMed]
    [Google Scholar]
  22. Crossman LC, Chen H, Cerdeño-Tárraga AM, Brooks K, Quail MA et al. A small predatory core genome in the divergent marine Bacteriovorax marinus SJ and the terrestrial Bdellovibrio bacteriovorus. ISME J 2013;7:148–160 [CrossRef][PubMed]
    [Google Scholar]
  23. Konstantinidis KT, Tiedje JM. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci USA 2005;102:2567–2572 [CrossRef][PubMed]
    [Google Scholar]
  24. Nakai R, Fujisawa T, Nakamura Y, Baba T, Nishijima M et al. Genome sequence and overview of Oligoflexus tunisiensis Shr3T in the eighth class Oligoflexia of the phylum Proteobacteria. Stand Genomic Sci 2016;11:90 [CrossRef][PubMed]
    [Google Scholar]
  25. Rendulic S, Jagtap P, Rosinus A, Eppinger M, Baar C et al. A predator unmasked: life cycle of Bdellovibrio bacteriovorus from a genomic perspective. Science 2004;303:689–692 [CrossRef][PubMed]
    [Google Scholar]
  26. Pasternak Z, Pietrokovski S, Rotem O, Gophna U, Lurie-Weinberger MN et al. By their genes ye shall know them: genomic signatures of predatory bacteria. ISME J 2013;7:756–769 [CrossRef][PubMed]
    [Google Scholar]
  27. Rodriguez-R LM, Konstantinidis KT. Bypassing cultivation to identify bacterial species. Microbe Magazine 2014;9:111–118 [CrossRef]
    [Google Scholar]
  28. Gupta RS. The phylogeny of proteobacteria: relationships to other eubacterial phyla and eukaryotes. FEMS Microbiol Rev 2000;24:367–402 [CrossRef][PubMed]
    [Google Scholar]
  29. Soo RM, Woodcroft BJ, Parks DH, Tyson GW, Hugenholtz P. Back from the dead; the curious tale of the predatory cyanobacterium Vampirovibrio chlorellavorus. Peer J 2015;3:e968 [CrossRef][PubMed]
    [Google Scholar]
  30. Karlin S, Brocchieri L, Mrázek J, Kaiser D. Distinguishing features of δ-proteobacterial genomes. Proc Natl Acad Sci USA 2006;103:11352–11357 [CrossRef][PubMed]
    [Google Scholar]
  31. Williams KP, Kelly DP. Proposal for a new class within the phylum Proteobacteria, Acidithiobacillia classis nov., with the type order Acidithiobacillales, and emended description of the class Gammaproteobacteria. Int J Syst Evol Microbiol 2013;63:2901–2906 [CrossRef][PubMed]
    [Google Scholar]
  32. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004;32:1792–1797 [CrossRef][PubMed]
    [Google Scholar]
  33. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016;33:1870–1874 [CrossRef][PubMed]
    [Google Scholar]
  34. Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 2007;56:564–577 [CrossRef][PubMed]
    [Google Scholar]
  35. Stamatakis A, Hoover P, Rougemont J. A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 2008;57:758–771 [CrossRef][PubMed]
    [Google Scholar]
  36. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A et al. MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 2012;61:539–542 [CrossRef][PubMed]
    [Google Scholar]
  37. Gromov BV, Mamkaeva KA. [Electron microscopic study of parasitism by Bdellovibrio chlorellavorus bacteria on cells of the green alga Chlorella vulgaris]. Tsitologiia 1972;14:256–260[PubMed]
    [Google Scholar]
  38. Gromov BV, Mamkaeva KA. [New genus of bacteria, Vampirovibrio, parasitizing chlorella and previously assigned to the genus Bdellovibrio]. Mikrobiologiia 1980;49:165–167[PubMed]
    [Google Scholar]
  39. di Rienzi SC, Sharon I, Wrighton KC, Koren O, Hug LA et al. The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria. Elife 2013;2:e01102 [CrossRef][PubMed]
    [Google Scholar]
  40. Soo RM, Skennerton CT, Sekiguchi Y, Imelfort M, Paech SJ et al. An expanded genomic representation of the phylum Cyanobacteria. Genome Biol Evol 2014;6:1031–1045 [CrossRef][PubMed]
    [Google Scholar]
  41. Yeoh YK, Sekiguchi Y, Parks DH, Hugenholtz P. Comparative genomics of Candidate phylum TM6 suggests that parasitism is widespread and ancestral in this lineage. Mol Biol Evol 2016;33:915–927 [CrossRef][PubMed]
    [Google Scholar]
  42. Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ et al. A new view of the tree of life. Nat Microbiol 2016;1:16048 [CrossRef][PubMed]
    [Google Scholar]
  43. Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 2014;12:635–645 [CrossRef][PubMed]
    [Google Scholar]
  44. McCauley EP, Haltli B, Kerr RG. Description of Pseudobacteriovorax antillogorgiicola gen. nov., sp. nov., a bacterium isolated from the gorgonian octocoral Antillogorgia elisabethae, belonging to the family Pseudobacteriovoracaceae fam. nov., within the order Bdellovibrionales. Int J Syst Evol Microbiol 2015;65:522–530 [CrossRef][PubMed]
    [Google Scholar]
  45. Green J. Carotenoid pigment in Spirobacillus cienkowskii metchnikoff, a pathogen of Cladocera. Nature 1959;183:56–57 [CrossRef][PubMed]
    [Google Scholar]
  46. Steinle P, Stucki G, Stettler R, Hanselmann KW. Aerobic mineralization of 2,6-dichlorophenol by Ralstonia sp. strain RK1. Appl Environ Microbiol 1998;64:2566–2571[PubMed]
    [Google Scholar]
  47. Stackebrandt E, Murray RGE, Truper HG. Proteobacteria classis nov., a name for the phylogenetic taxon that includes the "purple bacteria and their relatives". Int J Syst Bacteriol 1988;38:321–325 [CrossRef]
    [Google Scholar]
  48. Singer E, Emerson D, Webb EA, Barco RA, Kuenen JG et al. Mariprofundus ferrooxydans PV-1 the first genome of a marine Fe(II) oxidizing Zetaproteobacterium. PLoS One 2011;6:e25386 [CrossRef][PubMed]
    [Google Scholar]
  49. Garrity GM, Bell JA, Lilburn T. Order VII. Bdellovibrionales ord. nov. In Brenner DJ, Krieg NR, Staley JT, Garrity GM. (editors) Bergeys Manual of Systematic Bacteriology, 2nd ed. (The Proteobacteria), part C (The Alpha-, Beta-, Delta-, and Epsilonproteobacteria) 2005; pp.1040
    [Google Scholar]
  50. Kuever J, Rainey FA, Widdel F. Class VI. Deltaproteobacteria class nov. In Brenner DJ, Krieg NR, Staley JT, Garrity GM. (editors) Bergey’s Manual of Systematic Bacteriologyvol. 2 part C New York: Springer; 2005
    [Google Scholar]
  51. Garrity GM, Bell JA, Lilburn T. Order VII. Bdellovibrionales ord. nov. In Brenner DJ, Krieg NR, Staley JT, Garrity GM. (editors) Bergey’s Manual of Systematic Bacteriologyvol. 2 Part C New York: Springer; 2005
    [Google Scholar]
  52. Dirren S, Posch T. Promiscuous and specific bacterial symbiont acquisition in the amoeboid genus Nuclearia (Opisthokonta). FEMS Microbiol Ecol 2016;92:fiw105 [CrossRef][PubMed]
    [Google Scholar]
  53. Shaw AK, Halpern AL, Beeson K, Tran B, Venter JC et al. It's all relative: ranking the diversity of aquatic bacterial communities. Environ Microbiol 2008;10:2200–2210 [CrossRef][PubMed]
    [Google Scholar]
  54. Davidov Y, Jurkevitch E. Diversity and evolution of Bdellovibrio-and-like organisms (BALOs), reclassification of Bacteriovorax starrii as Peredibacter starrii gen. nov., comb. nov., and description of the Bacteriovorax–Peredibacter clade as Bacteriovoracaceae fam. nov. Int J Syst Evol Microbiol 2004;54:1439–1452 [CrossRef][PubMed]
    [Google Scholar]
  55. Koval SF, Williams HN, Stine OC. Reclassification of Bacteriovorax marinus as Halobacteriovorax marinus gen. nov., comb. nov. and Bacteriovorax litoralis as Halobacteriovorax litoralis comb. nov.; description of Halobacteriovoraceae fam. nov. in the class Deltaproteobacteria. Int J Syst Evol Microbiol 2015;65:593–597 [CrossRef][PubMed]
    [Google Scholar]
  56. Baer ML, Ravel J, Chun J, Hill RT, Williams HN. A proposal for the reclassification of Bdellovibrio stolpii and Bdellovibrio starrii into a new genus, Bacteriovorax gen. nov. as Bacteriovorax stolpii comb. nov. and Bacteriovorax starrii comb. nov., respectively. Int J Syst Evol Microbiol 2000;50:219–224 [CrossRef][PubMed]
    [Google Scholar]
  57. Stolp H, Starr MP. Bdellovibrio bacteriovorus gen. et sp. n., a predatory, ectoparasitic, and bacteriolytic microorganism. Antonie Van Leeuwenhoek 1963;29:217–248 [CrossRef][PubMed]
    [Google Scholar]
  58. Lambina VA, Afinogenova AV, Romaĭ Penabad S, Konovalova SM, Pushkareva AP. [Micavibrio admirandus gen. et sp. nov]. Mikrobiologiia 1982;51:114–117[PubMed]
    [Google Scholar]
  59. Garrity GM, Bell JA, Lilburn T, Family I. Bdellovibrionaceae fam. nov. In Brenner DJ KN, Staley JT, Garrity GM. (editors) Bergey’s Manual of Systematic Bacteriologyvol. 2 New York: Springer; 2005; pp.1040–1041
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.001965
Loading
/content/journal/ijsem/10.1099/ijsem.0.001965
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most Cited This Month

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