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Volume 66, Issue 3

Complete genome sequence and cell structure of , a Gram-negative spore-former within the phylum Free

Abstract

is a pleomorphic facultative anaerobe and the sole species in the class , which has tentatively been placed in the phylum . In the present study, the complete genome sequence of HC45 was obtained and analysed. The genome size was 3.82 Mbp and the DNA G+C content was 69.73 %. Phylogenetic analyses based on the 30S-50S ribosomal proteins and 23S rRNA gene consistently indicated that is phylogenetically isolated from the other members of the phylum . Ultrastructural observation revealed that possesses a Gram-negative-type cell wall and the capacity to form endospores. Accordingly, the genome has characteristics that are specific to Gram-negative bacteria and contains many genes that are involved in sporulation. On the other hand, several sporulation genes were absent from the genome although they have been regarded as essential for the endospore-forming system of members of the phylum . The B gene of possesses an intein sequence. The genome has a high percentage of GTG start codons and lacks several conserved genes related to cell division.

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2016-03-01
2024-04-25
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References

  1. Abecasis A. B., Serrano M., Alves R., Quintais L., Pereira-Leal J. B., Henriques A. O. 2013; A genomic signature and the identification of new sporulation genes. J Bacteriol 195:2101–2115 [View Article][PubMed]
     [Google Scholar]
  2. Aizawa S. 2014 The Flagellar World: Electron Microscopic Images of Bacterial Flagella and Related Surface Structures Waltham, MA: Academic Press, Elsevier;
     [Google Scholar]
  3. Ajithkumar B., Ajithkumar V. P., Iriye R., Doi Y., Sakai T. 2003; Spore-forming Serratia marcescens subsp. sakuensis subsp. nov., isolated from a domestic wastewater treatment tank. Int J Syst Evol Microbiol 53:253–258 [View Article][PubMed]
     [Google Scholar]
  4. Alauzet C., Marchandin H., Courtin P., Mory F., Lemée L., Pons J.-L., Chapot-Chartier M. P., Lozniewski A., Jumas-Bilak E. 2014; Multilocus analysis reveals diversity in the genus Tissierella: description of Tissierella carlieri sp. nov. in the new class Tissierellia classis nov. Syst Appl Microbiol 37:23–34 [View Article][PubMed]
     [Google Scholar]
  5. Barák I. 2013; Open questions about the function and evolution of bacterial Min systems. Front Microbiol 4:378 [View Article][PubMed]
     [Google Scholar]
  6. Beppu T., Ueda K. 2009; Family XVIII incertae sedis . In Bergey's Manual of Systematic Bacteriology, 2nd edn. vol. 3, The Firmicutes pp 1188–1190Edited by De Vos P., Garrity G. M., Jones D., Krieg N. R., Ludwig W., Rainey F. A., Schleifer K.-H., Whitman W. B. New York: Springer;
     [Google Scholar]
  7. Bernadac A., Gavioli M., Lazzaroni J. C., Raina S., Lloubès R. 1998; Escherichia coli tol-pal mutants form outer membrane vesicles. J Bacteriol 180:4872–4878[PubMed]
     [Google Scholar]
  8. Bland C., Ramsey T. L., Sabree F., Lowe M., Brown K., Kyrpides N. C., Hugenholtz P. 2007; CRISPR recognition tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinformatics 8:209 [View Article][PubMed]
     [Google Scholar]
  9. Chase D. G., Erlandsen S. L. 1976; Evidence for a complex life cycle and endospore formation in the attached, filamentous, segmented bacterium from murine ileum. J Bacteriol 127:572–583[PubMed]
     [Google Scholar]
  10. Chin C. S., Alexander D. H., Marks P., Klammer A. A., Drake J., Heiner C., Clum A., Copeland A., Huddleston J., other authors. 2013; Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 10:563–569 [View Article][PubMed]
     [Google Scholar]
  11. Ciccarelli F. D., Doerks T., von Mering C., Creevey C. J., Snel B, Bork P. 2006; Toward automatic reconstruction of a highly resolved tree of life. Science 311:1283–1287 [View Article][PubMed]
     [Google Scholar]
  12. da Costa M. S., Rainey F. A., Albuquerque L. 2009; Family XVII incertae sedis. Genus I. Sulfobacillus . In Bergey's Manual of Systematic Bacteriology, 2nd edn. vol. 3 The Firmicutes pp 1181–1184Edited by De Vos P., Garrity G. M., Jones D., Krieg N. R., Ludwig W., Rainey F. A., Schleifer K.-H., Whitman W. B. New York: Springer;
     [Google Scholar]
  13. Daniel R. A., Harry E. J., Katis V. L., Wake R. G., Errington J. 1998; Characterization of the essential cell division gene ftsL (yIID) of Bacillus subtilis and its role in the assembly of the division apparatus. Mol Microbiol 29:593–604 [View Article][PubMed]
     [Google Scholar]
  14. Deatherage B. L., Cookson B. T. 2012; Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect Immun 80:1948–1957 [View Article][PubMed]
     [Google Scholar]
  15. Egan A. J. F., Vollmer W. 2013; The physiology of bacterial cell division. Ann N Y Acad Sci 1277:8–28 [View Article][PubMed]
     [Google Scholar]
  16. Filippova S. N., Gorbatiuk E. V., Poglazova M. N., Soina V. S., Kuznetsov V. D., El'-Registan G. I. 2005; [Endospore formation by Streptomyces avermitilis in submerged culture]. Mikrobiologiia 74:204–214 (in Russian)
    [Google Scholar]
  17. Galperin M. Y. 2013; Genome diversity of spore-forming Firmicutes . Microbiol Spectr 1:TBS-0015-2012 [View Article][PubMed]
     [Google Scholar]
  18. Galperin M. Y., Mekhedov S. L., Puigbo P., Smirnov S., Wolf Y. I., Rigden D. J. 2012; Genomic determinants of sporulation in Bacilli and Clostridia: towards the minimal set of sporulation-specific genes. Environ Microbiol 14:2870–2890 [View Article][PubMed]
     [Google Scholar]
  19. Garrity G. M., Bell J. A., Lilburn T. 2005; The revised road map of the manual. In Bergey's Manual of Systematic Bacteriology, 2nd edn. vol. 2 The Proteobacteria, Part A pp 159–187Edited by Brenner D. J., Krieg N. R., Staley J. T., Garrity G. M. New York: Springer; [CrossRef]
     [Google Scholar]
  20. Ghosh J., Larsson P., Singh B., Pettersson B. M., Islam N. M., Sarkar S. N., Dasgupta S., Kirsebom L. A. 2009; Sporulation in mycobacteria. Proc Natl Acad Sci U S A 106:10781–10786 [View Article][PubMed]
     [Google Scholar]
  21. Girija K. R., Sasikala Ch., Ramana Ch. V., Spröer C., Takaichi S., Thiel V., Imhoff J. F. 2010; Rhodobacter johrii sp. nov., an endospore-producing cryptic species isolated from semi-arid tropical soils. Int J Syst Evol Microbiol 60:2099–2107 [View Article][PubMed]
     [Google Scholar]
  22. Jolley K. A., Bliss C. M., Bennett J. S., Bratcher H. B., Brehony C., Colles F. M., Wimalarathna H., Harrison O. B., Sheppard S. K., other authors. 2012; Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain. Microbiology 158:1005–1015[PubMed] [CrossRef]
     [Google Scholar]
  23. Kiss H., Nett M., Domin N., Martin K., Maresca J. A., Copeland A., Lapidus A., Lucas S., Berry K. W., other authors. 2011; Complete genome sequence of the filamentous gliding predatory bacterium Herpetosiphon aurantiacus type strain (114-95T). Stand Genomic Sci 5:356–370[PubMed] [CrossRef]
     [Google Scholar]
  24. Koch A. L. 2003; Were Gram-positive rods the first bacteria?. Trends Microbiol 11:166–170 [View Article][PubMed]
     [Google Scholar]
  25. Kuwahara T., Ogura Y., Oshima K., Kurokawa K., Ooka T., Hirakawa H., Itoh T., Nakayama-Imaohji H., Ichimura M., other authors. 2011; The lifestyle of the segmented filamentous bacterium: a non-culturable gut-associated immunostimulating microbe inferred by whole-genome sequencing. DNA Res 18:291–303 [View Article][PubMed]
     [Google Scholar]
  26. Lagesen K., Hallin P., Rødland E. A., Staerfeldt H. H., Rognes T., Ussery D. W. 2007; RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35:3100–3108 [View Article][PubMed]
     [Google Scholar]
  27. Lamont E. A., Bannantine J. P., Armién A., Ariyakumar D. S., Sreevatsan S. 2012; Identification and characterization of a spore-like morphotype in chronically starved Mycobacterium avium subsp. paratuberculosis cultures. PLoS One 7:e30648 [View Article][PubMed]
     [Google Scholar]
  28. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A., other authors. 2007; Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948 [View Article][PubMed]
     [Google Scholar]
  29. Lowe T. M., Eddy S. R. 1997; tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964 [View Article][PubMed]
     [Google Scholar]
  30. Ludwig W., Klenk H. P. 2001; Overview: a phylogenetic backbone and taxonomic framework for procaryotic systematics. In Bergey's Manual of Systematic Bacteriology, 2nd edn. vol. 1 The Archaea and the Deeply Branching and Phototrophic Bacteria pp 49–65Edited by Boone D. R., Castenholz R. W., Garrity G. M. New York: Springer; [CrossRef]
     [Google Scholar]
  31. Ludwig W., Schleifer K. H. 1999; Phylogeny of Bacteria beyond the 16S rRNA standard. ASM News 65:752–757
     [Google Scholar]
  32. Ludwig W., Strunk O., Klugbauer S., Klugbauer N., Weizenegger M., Neumaier J., Bachleitner M., Schleifer K. H. 1998; Bacterial phylogeny based on comparative sequence analysis. Electrophoresis 19:554–568 [View Article][PubMed]
     [Google Scholar]
  33. Ludwig W., Schleifer K. H., Whitman W. B. 2009; Revised road map to the phylum Firmicutes . In Bergey's Manual of Systematic Bacteriology, 2nd edn. vol. 3 The Firmicutes pp 1–14Edited by De Vos P., Garrity G. M., Jones D., Krieg N. R., Ludwig W., Rainey F. A., Schleifer K.-H., Whitman W. B. New York: Springer;
     [Google Scholar]
  34. MacGregor B. J., Biddle J. F., Teske A. 2013; Mobile elements in a single-filament orange Guaymas Basin Beggiatoa (“Candidatus Maribeggiatoa”) sp. draft genome: evidence for genetic exchange with cyanobacteria. Appl Environ Microbiol 79:3974–3985 [View Article][PubMed]
     [Google Scholar]
  35. Magee J. G., Ward A. C. 2012; Genus I. Mycobacterium . In Bergey's Manual of Systematic Bacteriology, 2nd edn. vol. 5 The Actinobacteria, part A pp 312–375Edited by Goodfellow M., Kämpfer P., Busse H.-J., Trujillo M. E., Suzuki K., Ludwig W., Whitman W. B. New York: Springer;
     [Google Scholar]
  36. Marchandin H., Teyssier C., Campos J., Jean-Pierre H., Roger F., Gay B., Carlier J.-P., Jumas-Bilak E. 2010; Negativicoccus succinicivorans gen. nov., sp. nov., isolated from human clinical samples, emended description of the family Veillonellaceae and description of Negativicutes classis nov., Selenomonadales ord. nov. and Acidaminococcaceae fam. nov. in the bacterial phylum Firmicutes . Int J Syst Evol Microbiol 60:1271–1279 [View Article][PubMed]
     [Google Scholar]
  37. Nakamura Y., Kaneko T., Sato S., Mimuro M., Miyashita H., Tsuchiya T., Sasamoto S., Watanabe A., Kawashima K., other authors. 2003; Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids. DNA Res 10:137–145 [View Article][PubMed]
     [Google Scholar]
  38. Newton-Foot M., Gey van Pittius N. C. 2013; The complex architecture of mycobacterial promoters. Tuberculosis (Edinb) 93:60–74 [View Article][PubMed]
     [Google Scholar]
  39. Noguchi H., Taniguchi T., Itoh T. 2008; MetaGeneAnnotator: detecting species-specific patterns of ribosomal binding site for precise gene prediction in anonymous prokaryotic and phage genomes. DNA Res 15:387–396 [View Article][PubMed]
     [Google Scholar]
  40. Opiyo S. O., Pardy R. L., Moriyama H., Moriyama E. N. 2010; Evolution of the Kdo2-lipid A biosynthesis in bacteria. BMC Evol Biol 10:362 [View Article][PubMed]
     [Google Scholar]
  41. Schleifer K. H. 2009; Phylum XIII. Firmicutes Gibbons and Murray 1978, 5 (Firmacutes [sic] Gibbons and Murray 1978, 5). In Bergey's Manual of Systematic Bacteriology, 2nd edn. vol. 3 The Firmicutes p 19Edited by De Vos P., Garrity G. M., Jones D., Krieg N. R., Ludwig W., Rainey F. A., Schleifer K.-H., Whitman W. B. New York: Springer;
     [Google Scholar]
  42. Singh B., Ghosh J., Islam N. M., Dasgupta S., Kirsebom L. A. 2010; Growth, cell division and sporulation in mycobacteria. Antonie van Leeuwenhoek 98:165–177 [View Article][PubMed]
     [Google Scholar]
  43. Sokolova T., Hanel J., Onyenwoke R. U., Reysenbach A. L., Banta A., Geyer R., González J. M., Whitman W. B., Wiegel J. 2007; Novel chemolithotrophic, thermophilic, anaerobic bacteria Thermolithobacter ferrireducens gen. nov., sp. nov. and Thermolithobacter carboxydivorans sp. nov. Extremophiles 11:145–157 [View Article][PubMed]
     [Google Scholar]
  44. Soucy S. M., Fullmer M. S., Papke R. T., Gogarten J. P. 2014; Inteins as indicators of gene flow in the halobacteria. Front Microbiol 5:299 [View Article][PubMed]
     [Google Scholar]
  45. Spanevello M. D., Patel B. K. C. 2009; Family XVII incertae sedis. Genus II. Thermaerobacter . In Bergey's Manual of Systematic Bacteriology, 2nd edn. vol. 3 The Firmicutes pp 1184–1187Edited by De Vos P., Garrity G. M., Jones D., Krieg N. R., Ludwig W., Rainey F. A., Schleifer K.-H., Whitman W. B. New York: Springer;
     [Google Scholar]
  46. Sugawara H., Ohyama A., Mori H., Kurokawa K. 2009; Microbial GenomeAnnotation Pipeline (MiGAP) for diverse users. In Proceedings of the 20th International Conference on Genome Informatics (GIW 2009) Yokohama, Japan, software demonstrations S001–1-2L
  47. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [View Article][PubMed]
     [Google Scholar]
  48. Traag B. A., Driks A., Stragier P., Bitter W., Broussard G., Hatfull G., Chu F., Adams K. N., Ramakrishnan L., Losick R. 2010; Do mycobacteria produce endospores?. Proc Natl Acad Sci U S A 107:878–881 [View Article][PubMed]
     [Google Scholar]
  49. Veiga H., Pinho M. G. 2012; Bacterial cell division: what it takes to divide a prokaryotic cell. Canal BQ 9:18–26
     [Google Scholar]
  50. Watanabe M., Kojima H., Fukui M. 2015; Limnochorda pilosa gen. nov., sp. nov., a moderately thermophilic, facultatively anaerobic, pleomorphic bacterium and proposal of Limnochordaceae fam. nov., Limnochordales ord. nov. and Limnochordia classis nov. in the phylum Firmicutes . Int J Syst Evol Microbiol 65:2378–2384 [View Article][PubMed]
     [Google Scholar]
  51. Yarza P., Ludwig W., Euzéby J., Amann R., Schleifer K. H., Glöckner F. O., Rosselló-Móra R. 2010; Update of the all-species living tree project based on 16S and 23S rRNA sequence analyses. Syst Appl Microbiol 33:291–299 [View Article][PubMed]
     [Google Scholar]
  52. Yutin N., Galperin M. Y. 2013; A genomic update on clostridial phylogeny: Gram-negative spore formers and other misplaced clostridia. Environ Microbiol 15:2631–2641[PubMed]
     [Google Scholar]
  53. Yutin N., Puigbò P., Koonin E. V., Wolf Y. I. 2012; Phylogenomics of prokaryotic ribosomal proteins. PLoS One 7:e36972 [View Article][PubMed]
     [Google Scholar]
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Complete genome sequence and cell structure of Limnochorda pilosa, a Gram-negative spore-former within the phylum Firmicutes
Int J Syst Evol Microbiol 66, 1330 (2016); https://doi.org/10.1099/ijsem.0.000881
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