gen. nov., sp. nov., a member of the family isolated from an Antarctic lichen Free

Abstract

Two Gram-stain-negative, facultative anaerobic, chemoheterotrophic, pink-coloured, rod-shaped and non-motile bacterial strains, PAMC 26568 and PAMC 26569, were isolated from an Antarctic lichen. Phylogenetic analysis based on 16S rRNA gene sequences revealed that strains PAMC 26568 and PAMC 26569 belong to the family and the most closely related species are (96.1 %), (95.9 %) and (95.7 %). Phylogenomic and genomic relatedness analyses showed that strains PAMC 26568 and PAMC 26569 are clearly distinguished from other genera in the family by average nucleotide identity values (<72.8 %) and the genome-to-genome distance values (<22.5 %). Genomic analysis revealed that strains PAMC 26568 and PAMC 26569 do not contain genes involved in atmospheric nitrogen fixation and utilization of sole carbon compounds such as methane and methanol. Instead, strains PAMC 26568 and PAMC 26569 possess genes to utilize nitrate and nitrite and certain monosaccharides and disaccharides. The major fatty acids (>10 %) are summed feature 8 (C ω7 and/or C ω6; 40.3–40.4 %), C 2OH (22.7–23.7 %) and summed feature 2 (C 3OH and/or C iso I; 12.0 % in PAMC 26568). The major respiratory quinone is Q-10. The genomic DNA G+C content of PAMC 26568 and PAMC 26569 is 64.6 %. Their distinct phylogenetic position and some physiological characteristics distinguish strains PAMC 26568 and PAMC 26569 from other genera in the family supporting the proposal of gen. nov., with the type species sp. nov. (type strain, PAMC 26569=KCCM 43315=JCM 33604).

Funding
This study was supported by the:
  • Korea Polar Research Institute (Award PE20170)
    • Principle Award Recipient: Not Applicable
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004495
2020-10-09
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/70/11/5918.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.004495&mimeType=html&fmt=ahah

References

  1. De Bary A. Die erscheinung der symbiose: Verlag von Karl J. Trübner; 1879
  2. Nash TH. Lichen Biology New York: Cambridge University Press; 2008
    [Google Scholar]
  3. Lawrey JD, Diederich P. Lichenicolous fungi: interactions, evolution, and biodiversity. Bryologist 2003; 106:80–120 [View Article]
    [Google Scholar]
  4. González I, Ayuso-Sacido A, Anderson A, Genilloud O. Actinomycetes isolated from lichens: evaluation of their diversity and detection of biosynthetic gene sequences. FEMS Microbiol Ecol 2005; 54:401–415 [View Article][PubMed]
    [Google Scholar]
  5. Liba C, Ferrara F, Manfio G, Fantinatti-Garboggini F, Albuquerque R et al. Nitrogen‐fixing chemo-organotrophic bacteria isolated from cyanobacteria-deprived lichens and their ability to solubilize phosphate and to release amino acids and phytohormones. J Appl Microbiol 2006; 101:1076–1086 [View Article][PubMed]
    [Google Scholar]
  6. Cardinale M, Vieira de Castro J, Müller H, Berg G, Grube M. In situ analysis of the bacterial community associated with the reindeer lichen Cladonia arbuscula reveals predominance of Alphaproteobacteria. FEMS Microbiol Ecol 2008; 66:63–71 [View Article][PubMed]
    [Google Scholar]
  7. Grube M, Cardinale M, de Castro JV, Müller H, Berg G. Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME J 2009; 3:1105–1115 [View Article][PubMed]
    [Google Scholar]
  8. Bates ST, Cropsey GW, Caporaso JG, Knight R, Fierer N. Bacterial communities associated with the lichen symbiosis. Appl Environ Microbiol 2011; 77:1309–1314 [View Article][PubMed]
    [Google Scholar]
  9. Hodkinson BP, Gottel NR, Schadt CW, Lutzoni F. Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome. Environ Microbiol 2012; 14:147–161 [View Article][PubMed]
    [Google Scholar]
  10. Lee YM, Kim EH, Lee HK, Hong SG. Biodiversity and physiological characteristics of Antarctic and Arctic lichens-associated bacteria. World J Microbiol Biotechnol 2014; 30:2711–2721 [View Article][PubMed]
    [Google Scholar]
  11. Biosca EG, Flores R, Santander RD, Díez-Gil JL, Barreno E. Innovative approaches using lichen enriched media to improve isolation and culturability of lichen associated bacteria. PLoS One 2016; 11:e0160328 [View Article][PubMed]
    [Google Scholar]
  12. Grube M, Cernava T, Soh J, Fuchs S, Aschenbrenner I et al. Exploring functional contexts of symbiotic sustain within lichen-associated bacteria by comparative omics. ISME J 2015; 9:412–424 [View Article][PubMed]
    [Google Scholar]
  13. Park CH, Kim KM, Kim OS, Jeong G, Hong SG. Bacterial communities in Antarctic lichens. Antarct Sci 20161–7
    [Google Scholar]
  14. Noh HJ, Lee YM, Park CH, Lee HK, Cho JC et al. Microbiome in Cladonia squamosa is vertically stratified according to microclimatic conditions. Front Microbiol 2020; 11:268 [View Article][PubMed]
    [Google Scholar]
  15. Printzen C, Fernández-Mendoza F, Muggia L, Berg G, Grube M. Alphaproteobacterial communities in geographically distant populations of the lichen Cetraria aculeata. FEMS Microbiol Ecol 2012; 82:316–325 [View Article][PubMed]
    [Google Scholar]
  16. Sierra MA, Danko DC, Sandoval TA, Pishchany G, Moncada B et al. The microbiomes of seven lichen genera reveal host specificity, a reduced core community and potential as source of antimicrobials. Front Microbiol 2020; 11:398 [View Article][PubMed]
    [Google Scholar]
  17. Brown BP, Wernegreen JJ. Genomic erosion and extensive horizontal gene transfer in gut-associated Acetobacteraceae. BMC Genomics 2019; 20:1–15 [View Article]
    [Google Scholar]
  18. Pedraza RO. Recent advances in nitrogen-fixing acetic acid bacteria. Int J Food Microbiol 2008; 125:25–35 [View Article][PubMed]
    [Google Scholar]
  19. Loganathan P, Nair S. Swaminathania salitolerans gen. nov., sp. nov., a salt-tolerant, nitrogen-fixing and phosphate-solubilizing bacterium from wild rice (Porteresia coarctata Tateoka). Int J Syst Evol Microbiol 2004; 54:1185–1190 [View Article][PubMed]
    [Google Scholar]
  20. Gillis M, Kersters K, Hoste B, Janssens D, Kroppenstedt R et al. Acetobacter diazotrophicus sp. nov., a nitrogen-fixing acetic acid bacterium associated with sugarcane. Int J Syst Evol Microbiol 1989; 39:361–364
    [Google Scholar]
  21. Muthukumarasamy R, Cleenwerck I, Revathi G, Vadivelu M, Janssens D et al. Natural association of Gluconacetobacter diazotrophicus and diazotrophic Acetobacter peroxydans with wetland rice. Syst Appl Microbiol 2005; 28:277–286 [View Article][PubMed]
    [Google Scholar]
  22. Lane D. 16S/23S rRNA sequencing. Nucleic Acid Techniques in Bacterial Systematics 1991
    [Google Scholar]
  23. Yoon SH, Ha SM, 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]
  24. Jeon YS, Chung H, Park S, Hur I, Lee JH et al. jPHYDIT: a JAVA-based integrated environment for molecular phylogeny of ribosomal RNA sequences. Bioinformatics 2005; 21:3171–3173 [View Article][PubMed]
    [Google Scholar]
  25. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article][PubMed]
    [Google Scholar]
  26. 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 [View Article][PubMed]
    [Google Scholar]
  27. 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][PubMed]
    [Google Scholar]
  28. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article][PubMed]
    [Google Scholar]
  29. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article][PubMed]
    [Google Scholar]
  30. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article][PubMed]
    [Google Scholar]
  31. Haft DH, DiCuccio M, Badretdin A, Brover V, Chetvernin V et al. RefSeq: an update on prokaryotic genome annotation and curation. Nucleic Acids Res 2018; 46:D851–D860 [View Article][PubMed]
    [Google Scholar]
  32. Moriya Y, Itoh M, Okuda S, Kanehisa M. KAAS: KEGG automatic annotation server. Genome Informatics 2005; 5:2005
    [Google Scholar]
  33. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010; 26:2460–2461 [View Article][PubMed]
    [Google Scholar]
  34. Yoon S-H, Ha SM, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article][PubMed]
    [Google Scholar]
  35. Auch AF, von Jan M, Klenk H-P, Göker M. Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2010; 2:117–134 [View Article][PubMed]
    [Google Scholar]
  36. Rodriguez-R LM, Konstantinidis KT. Bypassing cultivation to identify bacterial species. Microbe 2014; 9:111–118 [View Article]
    [Google Scholar]
  37. Qin Q-L, Xie B-B, Zhang X-Y, Chen X-L, Zhou B-C et al. A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 2014; 196:2210–2215 [View Article][PubMed]
    [Google Scholar]
  38. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 2009; 106:19126–19131 [View Article][PubMed]
    [Google Scholar]
  39. Rosselló-Mora R, Amann R. The species concept for prokaryotes. FEMS Microbiol Rev 2001; 25:39–67 [View Article][PubMed]
    [Google Scholar]
  40. 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]
  41. Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the genome taxonomy database. Bioinformatics 2020; 36:1925–1927
    [Google Scholar]
  42. Kovacs N. Identification of Pseudomonas pyocyanea by the oxidase reaction. Nature 1956; 178:703 [View Article][PubMed]
    [Google Scholar]
  43. Kersters K, De Vos P, Gillis M, Swings J, Vandamme P et al. Introduction to the Proteobacteria. The Prokaryotes 2006; 5:3–37
    [Google Scholar]
  44. Sasser M. Bacterial Identification by Gas Chromatographic Analysis of Fatty Acids Methyl Esters (GC-FAME) Newark, NY: Microbial; 2006
    [Google Scholar]
  45. Collins MD, Jones D. Distribution of isoprenoid quinone structural types in bacteria and their taxonomic implication. Microbiol Rev 1981; 45:316–354 [View Article][PubMed]
    [Google Scholar]
  46. Nishijima M, Tazato N, Handa Y, Tomita J, Kigawa R et al. Gluconacetobacter tumulisoli sp. nov., Gluconacetobacter takamatsuzukensis sp. nov. and Gluconacetobacter aggeris sp. nov., isolated from Takamatsuzuka Tumulus samples before and during the dismantling work in 2007. Int J Syst Evol Microbiol 2013; 63:3981–3988 [View Article][PubMed]
    [Google Scholar]
  47. Franke IH, Fegan M, Hayward C, Leonard G, Stackebrandt E et al. Description of Gluconacetobacter sacchari sp. nov., a new species of acetic acid bacterium isolated from the leaf sheath of sugar cane and from the pink sugar-cane mealy bug. Int J Syst Bacteriol 1999; 49:1681–1693 [View Article][PubMed]
    [Google Scholar]
  48. Gosselé F, Swings J, Kersters K, Pauwels P, De Ley J. Numerical analysis of phenotypic features and protein gel electrophoregrams of a wide variety of Acetobacter strains. Proposal for the improvement of the taxonomy of the genus Acetobacter Beijerinck 1898, 215. Syst Appl Microbiol 1983; 4:338–368 [View Article][PubMed]
    [Google Scholar]
  49. Tazato N, Nishijima M, Handa Y, Kigawa R, Sano C et al. Gluconacetobacter tumulicola sp. nov. and Gluconacetobacter asukensis sp. nov., isolated from the stone chamber interior of the Kitora Tumulus. Int J Syst Evol Microbiol 2012; 62:2032–2038 [View Article][PubMed]
    [Google Scholar]
  50. Fuentes-Ramírez LE, Bustillos-Cristales R, Tapia-Hernández A, Jiménez-Salgado T, Wang ET et al. Novel nitrogen-fixing acetic acid bacteria, Gluconacetobacter johannae sp. nov. and Gluconacetobacter azotocaptans sp. nov., associated with coffee plants. Int J Syst Evol Microbiol 2001; 51:1305–1314 [View Article][PubMed]
    [Google Scholar]
  51. Lisdiyanti P, Kawasaki H, Widyastuti Y, Saono S, Seki T et al. Kozakia baliensis gen. nov., sp. nov., a novel acetic acid bacterium in the alpha-proteobacteria. Int J Syst Evol Microbiol 2002; 52:813–818 [View Article][PubMed]
    [Google Scholar]
  52. Urakami T, Tamaoka J, Suzuki K-I, Komagata K. Acidomonas gen. nov., incorporating Acetobacter methanolicus as Acidomonas methanolica comb. nov. Int J Syst Bacteriol 1989; 39:50–55 [View Article]
    [Google Scholar]
  53. Yukphan P, Malimas T, Muramatsu Y, Takahashi M, Kaneyasu M et al. Ameyamaea chiangmaiensis gen. nov., sp. nov., an acetic acid bacterium in the α -Proteobacteria. Biosci Biotechnol Biochem 2009; 73:2156–2162 [View Article]
    [Google Scholar]
  54. Vu HTL, Malimas T, Chaipitakchonlatarn W, Yukphan P, Bui UTT et al. Tanticharoenia aidae sp. nov., for acetic acid bacteria isolated in Vietnam. Ann Microbiol 2016; 66:417–423
    [Google Scholar]
  55. Vu HTL, Yukphan P, Chaipitakchonlatarn W, Malimas T, Muramatsu Y et al. Nguyenibacter vanlangensis gen. nov., sp. nov., an unusual acetic acid bacterium in the α-Proteobacteria. J Gen Appl Microbiol 2013; 59:153–166 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004495
Loading
/content/journal/ijsem/10.1099/ijsem.0.004495
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed