1887

Abstract

The genus (family ) is phylogenetically subdivided into at least four subclusters. One of those, subcluster PnecC, was recognized as a cryptic species complex. Here we test by comparative genome analyses whether subcluster PnecD, currently solely represented by the species , also represents such a cryptic species complex. The genome sequences of the two strains, MWH-MoIso2 and MWH-VicM1, were determined. The latter strain was also characterized in the previous description of . These two strains originate from a temperate lake located in Austria and from the large tropical Lake Victoria located in East Africa, respectively. Strains MWH-MoIso2 and MWH-VicM1 possess quite small genomes of 1.78 and 1.63 Mbp, respectively, and share similar G+C values of 44.1 and 43.1 mol%, respectively. Both strains encode only a single copy of the ribosomal operon, and their 16S rRNA genes differ only in four positions, equalling a sequence similarity of 99.74 %. Both genomes possess characteristics indicating evolutionary genome streamlining, such as high coding densities of 93.9 and 94.6 % of bases, respectively. Average nucleotide identity (ANI) comparisons of the genomes of the two strains resulted in a value of 78.4 %, suggesting that each of the strains represents a separate species. Our investigation suggests that PnecD represents an additional cryptic species complex within the genus that was not resolved by 16S rRNA gene sequence analyses. We propose reclassification of strain MWH-VicM1 as sp. nov., with type strain MWH-VicM1(=DSM 21486=JCM 32005).

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2017-12-01
2019-12-11
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References

  1. Heckmann K, Schmidt HJ. Polynucleobacter necessarius gen. nov., sp. nov., an obligately endosymbiotic bacterium living in the cytoplasm of Euplotes aediculatus. Int J Syst Bacteriol 1987;37:456–457 [CrossRef]
    [Google Scholar]
  2. Bahr M, Hobbie JE, Sogin ML. Bacterial diversity in an arctic lake: a freshwater SAR11 cluster. Aquatic Microbial Ecology 1996;11:271–277 [CrossRef]
    [Google Scholar]
  3. Wu QL, Hahn MW. Differences in structure and dynamics of Polynucleobacter communities in a temperate and a subtropical lake, revealed at three phylogenetic levels. FEMS Microbiol Ecol 2006;57:67–79 [CrossRef][PubMed]
    [Google Scholar]
  4. Crump BC, Peterson BJ, Raymond PA, Amon RM, Rinehart A et al. Circumpolar synchrony in big river bacterioplankton. Proc Natl Acad Sci USA 2009;106:21208–21212 [CrossRef][PubMed]
    [Google Scholar]
  5. Jezberová J, Jezbera J, Brandt U, Lindström ES, Langenheder S et al. Ubiquity of Polynucleobacter necessarius ssp. asymbioticus in lentic freshwater habitats of a heterogeneous 2000 km2 area. Environ Microbiol 2010;12:658–669 [CrossRef][PubMed]
    [Google Scholar]
  6. Hahn MW. Isolation of strains belonging to the cosmopolitan Polynucleobacter necessarius cluster from freshwater habitats located in three climatic zones. Appl Environ Microbiol 2003;69:5248–5254 [CrossRef][PubMed]
    [Google Scholar]
  7. Burkert U, Warnecke F, Babenzien D, Zwirnmann E, Pernthaler J. Members of a readily enriched β-proteobacterial clade are common in surface waters of a humic lake. Appl Environ Microbiol 2003;69:6550–6559 [CrossRef][PubMed]
    [Google Scholar]
  8. Vannini C, Pöckl M, Petroni G, Wu QL, Lang E et al. Endosymbiosis in statu nascendi: close phylogenetic relationship between obligately endosymbiotic and obligately free-living Polynucleobacter strains (Betaproteobacteria). Environ Microbiol 2007;9:347–359 [CrossRef][PubMed]
    [Google Scholar]
  9. 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. necessarius subsp. asymbioticus subsp. nov. Int J Syst Evol Microbiol 2009;59:2002–2009 [CrossRef][PubMed]
    [Google Scholar]
  10. Boscaro V, Felletti M, Vannini C, Ackerman MS, Chain PS et al. Polynucleobacter necessarius, a model for genome reduction in both free-living and symbiotic bacteria. Proc Natl Acad Sci USA 2013;110:18590–18595 [CrossRef][PubMed]
    [Google Scholar]
  11. 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 [CrossRef][PubMed]
    [Google Scholar]
  12. Watanabe K, Komatsu N, Kitamura T, Ishii Y, Park HD et al. Ecological niche separation in the Polynucleobacter subclusters linked to quality of dissolved organic matter: a demonstration using a high sensitivity cultivation-based approach. Environ Microbiol 2012;14:2511–2525 [CrossRef][PubMed]
    [Google Scholar]
  13. Hahn MW, Jezberová 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 [CrossRef][PubMed]
    [Google Scholar]
  14. 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]
  15. Hahn MW, Karbon G, Koll U, Schmidt J, Lang E. Polynucleobacter sphagniphilus sp. nov. a planktonic freshwater bacterium isolated from an acidic and humic freshwater habitat. Int J Syst Evol Microbiol 2017;67:3261–3267 [CrossRef][PubMed]
    [Google Scholar]
  16. Hahn MW, Huymann LR, Koll U, Schmidt J, Lang E et al. Polynucleobacter wuianus sp. nov., a free-living freshwater bacterium affiliated with the cryptic species complex PnecC. Int J Syst Evol Microbiol 2017;67:379–385 [CrossRef][PubMed]
    [Google Scholar]
  17. Hahn MW, Lang E, Brandt U, Lünsdorf H, Wu QL et al. Polynucleobacter cosmopolitanus sp. nov., free-living planktonic bacteria inhabiting freshwater lakes and rivers. Int J Syst Evol Microbiol 2010;60:166–173 [CrossRef][PubMed]
    [Google Scholar]
  18. 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]
  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. Whitman WB, Woyke T, Klenk HP, Zhou Y, Lilburn TG et al. Genomic encyclopedia of bacterial and archaeal type strains, phase III: the genomes of soil and plant-associated and newly described type strains. Stand Genomic Sci 2015;10:26 [CrossRef][PubMed]
    [Google Scholar]
  21. 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]
  22. Huntemann M, Ivanova NN, Mavromatis K, Tripp HJ, Paez-Espino D et al. The standard operating procedure of the DOE-JGI Microbial Genome Annotation Pipeline (MGAP v.4). Stand Genomic Sci 2015;10:86 [CrossRef][PubMed]
    [Google Scholar]
  23. Chen IM, Markowitz VM, Palaniappan K, Szeto E, Chu K et al. Supporting community annotation and user collaboration in the integrated microbial genomes (IMG) system. BMC Genomics 2016;17:307 [CrossRef][PubMed]
    [Google Scholar]
  24. Hoetzinger M, Schmidt J, Jezberová J, Koll U, Hahn MW. Microdiversification of a pelagic Polynucleobacter species is mainly driven by acquisition of genomic islands from a partially interspecific gene pool. Appl Environ Microbiol 2017;83:e02266-16 [CrossRef][PubMed]
    [Google Scholar]
  25. Hahn MW, Scheuerl T, Jezberová J, Koll U, Jezbera J et al. The passive yet successful way of planktonic life: genomic and experimental analysis of the ecology of a free-living polynucleobacter population. PLoS One 2012;7:e32772 [CrossRef][PubMed]
    [Google Scholar]
  26. Boscaro V, Kolisko M, Felletti M, Vannini C, Lynn DH et al. Parallel genome reduction in symbionts descended from closely related free-living bacteria. Nat Ecol Evol 2017;1:1160–1167 [CrossRef]
    [Google Scholar]
  27. Hahn MW, Koll U, Karbon G, Schmidt J, Lang E. Polynucleobacter aenigmaticus sp. nov. isolated from the permanently anoxic monimolimnion of a temperate meromictic lake. Int J Syst Evol Microbiol in press
    [Google Scholar]
  28. Salcher MM, Neuenschwander SM, Posch T, Pernthaler J. The ecology of pelagic freshwater methylotrophs assessed by a high-resolution monitoring and isolation campaign. Isme J 2015;9:2442–2453 [CrossRef][PubMed]
    [Google Scholar]
  29. Giovannoni SJ, Hayakawa DH, Tripp HJ, Stingl U, Givan SA et al. The small genome of an abundant coastal ocean methylotroph. Environ Microbiol 2008;10:1771–1782 [CrossRef][PubMed]
    [Google Scholar]
  30. 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]
  31. 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 [CrossRef][PubMed]
    [Google Scholar]
  32. Hao Z, Li L, Liu J, Ren Y, Wang L et al. Genome sequence of a freshwater low-nucleic-acid-content bacterium, Betaproteobacterium strain CB. Genome Announc 2013;1:e00135-13 [CrossRef][PubMed]
    [Google Scholar]
  33. Zaremba-Niedzwiedzka K, Caceres EF, Saw JH, Bäckström D, Juzokaite L et al. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 2017;541:353–358 [CrossRef][PubMed]
    [Google Scholar]
  34. Janssen PJ, van Houdt R, Moors H, Monsieurs P, Morin N et al. The complete genome sequence of Cupriavidus metallidurans strain CH34, a master survivalist in harsh and anthropogenic environments. PLoS One 2010;5:e10433 [CrossRef][PubMed]
    [Google Scholar]
  35. Amadou C, Pascal G, Mangenot S, Glew M, Bontemps C et al. Genome sequence of the beta-rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia. Genome Res 2008;18:1472–1483 [CrossRef][PubMed]
    [Google Scholar]
  36. 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]
  37. Hahn MW, Koll U, Jezberová J, Camacho A. Global phylogeography of pelagic Polynucleobacter bacteria: restricted geographic distribution of subgroups, isolation by distance and influence of climate. Environ Microbiol 2015;17:829–840 [CrossRef][PubMed]
    [Google Scholar]
  38. Hahn MW, Lang E, Tarao M, Brandt U. Polynucleobacter rarus sp. nov., a free-living planktonic bacterium isolated from an acidic lake. Int J Syst Evol Microbiol 2011;61:781–787 [CrossRef][PubMed]
    [Google Scholar]
  39. Hahn MW, Minasyan A, Lang E, Koll U, Spröer C. Polynucleobacter difficilis sp. nov., a planktonic freshwater bacterium affiliated with subcluster B1 of the genus Polynucleobacter. Int J Syst Evol Microbiol 2012;62:376–383 [CrossRef][PubMed]
    [Google Scholar]
  40. Hahn MW, Lang E, Brandt U, Spröer C. Polynucleobacter acidiphobus sp. nov., a representative of an abundant group of planktonic freshwater bacteria. Int J Syst Evol Microbiol 2011;61:788–794 [CrossRef][PubMed]
    [Google Scholar]
  41. 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 [CrossRef][PubMed]
    [Google Scholar]
  42. 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]
  43. 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 [CrossRef][PubMed]
    [Google Scholar]
  44. Hahn MW, Pöckl M, Wu QL. Low intraspecific diversity in a polynucleobacter subcluster population numerically dominating bacterioplankton of a freshwater pond. Appl Environ Microbiol 2005;71:4539–4547 [CrossRef][PubMed]
    [Google Scholar]
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