1887

Abstract

Two aerobic and obligately acidophilic bacteria, designated 4G-K13 and 4Y35, were isolated from the forest soil sampled at Dinghushan Biosphere Reserve, Guangdong Province, PR China. These two strains were Gram-stain-negative, non-motile and short rods that multiplied by binary division. Strains 4G-K13 and 4Y35 had the highest 16S rRNA gene sequence similarity of 97.0 and 97.2 % to DSM 103733 and SBC82, respectively. Phylogenetic trees based on the 16S rRNA gene and whole genome sequences showed consistently that these two strains formed a major clade with members of the genera , , and in the family , but each occupied an unique position. In both the UBCG and the PhyloPhlAn phylogenomic trees, strains 4G-K13 and 4Y35 congruently formed a highly supported subclade with DSM 11244 and DSM 27394, respectively. The major fatty acids (>5 %) of strain 4G-K13 were iso-C, iso-C, summed feature 3 (C 7 and/or C 6) and summed feature 9 (iso-C 9 and/or C 10-methyl), while that of strain 4Y35 were C, C 9, iso-C, summed feature 3 (C 7 and/or C 6) and summed feature 9 (iso-C 9 and/or C 10-methyl). Strain 4G-K13 contained phosphatidylethanolamine, four unidentified phospholipids, four glycolipids, two unidentified aminolipids and two unknown lipids, while strain 4Y35 had phosphatidylethanolamine, three unidentified phospholipids, two glycolipids, five unidentified aminolipids and one unknown polar lipid. The DNA G+C contents of 4G-K13 and 4Y35 were 60.5 and 55.8 mol%, respectively. Based on all these phylogenetic, physiological and chemotaxonomic data, we suggest that strains 4G-K13 and 4Y35 represent two novel species of two novel genera in the family , for which the names gen. nov., sp. nov. (type strain: 4G-K13=GDMCC 1.1195=NBRC 113249) and gen. nov., sp. nov. (type strain: 4Y35=KACC 21728=NBRC 114261) are proposed. We also propose to reclassify and as gen. nov., comb. nov. and comb. nov., respectively, based mainly on the results of phylogenomic analysis.

Funding
This study was supported by the:
  • Guangdong Province Science and Technology Innovation Strategy Special Fund (Award 2018B020205003)
    • Principle Award Recipient: Li-hongQiu
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2022-06-09
2024-04-28
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References

  1. Janssen PH. Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 2006; 72:1719–1728 [View Article] [PubMed]
    [Google Scholar]
  2. Hugenholtz P, Goebel BM, Pace NR. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 1998; 180:4765–4774 [View Article] [PubMed]
    [Google Scholar]
  3. Ludwig W, Bauer SH, Bauer M, Held I, Kirchhof G et al. Detection and in situ identification of representatives of a widely distributed new bacterial phylum. FEMS Microbiol Lett 1997; 153:181–190 [View Article] [PubMed]
    [Google Scholar]
  4. Chow ML, Radomski CC, McDermott JM, Davies J, Axelrood PE et al. Molecular characterization of bacterial diversity in Lodgepole pine (Pinus contorta) rhizosphere soils from British Columbia forest soils differing in disturbance and geographic source. FEMS Microbiol Ecol 2002; 42:347–357 [View Article] [PubMed]
    [Google Scholar]
  5. Pointing SB, Chan Y, Lacap DC, Lau MCY, Jurgens JA et al. Highly specialized microbial diversity in hyper-arid polar desert. Proc Natl Acad Sci U S A 2009; 106:19964–19969 [View Article] [PubMed]
    [Google Scholar]
  6. Hobel CFV, Marteinsson VT, Hreggvidsson GO, Kristjánsson JK. Investigation of the microbial ecology of intertidal hot springs by using diversity analysis of 16S rRNA and chitinase genes. Appl Environ Microbiol 2005; 71:2771–2776 [View Article] [PubMed]
    [Google Scholar]
  7. Barns SM, Cain EC, Sommerville L, Kuske CR. Acidobacteria phylum sequences in uranium-contaminated subsurface sediments greatly expand the known diversity within the phylum. Appl Environ Microbiol 2007; 73:3113–3116 [View Article] [PubMed]
    [Google Scholar]
  8. Barns SM, Cain EC, Sommerville L, Kuske CR. Acidobacteria phylum sequences in uranium-contaminated subsurface sediments greatly expand the known diversity within the phylum. Appl Environ Microbiol 2007; 73:3113–3116 [View Article] [PubMed]
    [Google Scholar]
  9. Dedysh SN, Yilmaz P. Refining the taxonomic structure of the phylum Acidobacteria. Int J Syst Evol Microbiol 2018; 68:3796–3806 [View Article] [PubMed]
    [Google Scholar]
  10. Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R et al. A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 2009; 3:442–453 [View Article] [PubMed]
    [Google Scholar]
  11. Pankratov TA, Kirsanova LA, Kaparullina EN, Kevbrin VV, Dedysh SN. Telmatobacter bradus gen. nov., sp. nov., a cellulolytic facultative anaerobe from subdivision 1 of the Acidobacteria, and emended description of Acidobacterium capsulatum Kishimoto et al. 1991. Int J Syst Evol Microbiol 2012; 62:430–437 [View Article] [PubMed]
    [Google Scholar]
  12. Pankratov TA, Dedysh SN. Granulicella paludicola gen. nov., sp. nov., Granulicella pectinivorans sp. nov., Granulicella aggregans sp. nov. and Granulicella rosea sp. nov., acidophilic, polymer-degrading acidobacteria from Sphagnum peat bogs. Int J Syst Evol Microbiol 2010; 60:2951–2959 [View Article]
    [Google Scholar]
  13. Okamura K, Kawai A, Yamada T, Hiraishi A. Acidipila rosea gen. nov., sp. nov., an acidophilic chemoorganotrophic bacterium belonging to the phylum Acidobacteria. FEMS Microbiol Lett 2011; 317:138–142 [View Article]
    [Google Scholar]
  14. Lladó S, Benada O, Cajthaml T, Baldrian P, García-Fraile P. Silvibacterium bohemicum gen. nov. sp. nov., an acidobacterium isolated from coniferous soil in the Bohemian Forest National Park. Syst Appl Microbiol 2016; 39:14–19 [View Article]
    [Google Scholar]
  15. Kulichevskaya IS, Kostina LA, Valášková V, Rijpstra WIC, Sinninghe Damsté JS et al. Acidicapsa borealis gen. nov., sp. nov. and Acidicapsa ligni sp. nov., subdivision 1 Acidobacteria from Sphagnum peat and decaying wood. Int J Syst Evol Microbiol 2012; 62:1512–1520 [View Article]
    [Google Scholar]
  16. Koch IH, Gich F, Dunfield PF, Overmann J. Edaphobacter modestus gen. nov., sp. nov., and Edaphobacter aggregans sp. nov., acidobacteria isolated from alpine and forest soils. Int J Syst Evol Microbiol 2008; 58:1114–1122 [View Article]
    [Google Scholar]
  17. Kishimoto N, Kosako Y, Tano T. Acidobacterium capsulatum gen. nov., sp. nov.: An acidophilic chemoorganotrophic bacterium containing menaquinone from acidic mineral environment. Current Microbiology 1991; 22:1–7 [View Article]
    [Google Scholar]
  18. García-Fraile P, Benada O, Cajthaml T, Baldrian P, Lladó S et al. Terracidiphilus gabretensis gen. nov., sp. nov., an abundant and active forest soil acidobacterium important in organic matter transformation. Appl Environ Microbiol 2016; 82:560–569 [View Article]
    [Google Scholar]
  19. Foesel BU, Mayer S, Luckner M, Wanner G, Rohde M et al. Occallatibacter riparius gen. nov., sp. nov. and Occallatibacter savannae sp. nov., acidobacteria isolated from Namibian soils, and emended description of the family Acidobacteriaceae. Int J Syst Evol Microbiol 2016; 66:219–229 [View Article]
    [Google Scholar]
  20. Dedysh SN, Kulichevskaya IS, Serkebaeva YM, Mityaeva MA, Sorokin VV et al. Bryocella elongata gen. nov., sp. nov., a member of subdivision 1 of the Acidobacteria isolated from a methanotrophic enrichment culture, and emended description of Edaphobacter aggregans Koch et al. 2008. Int J Syst Evol Microbiol 2012; 62:654–664 [View Article] [PubMed]
    [Google Scholar]
  21. Belova SE, Ravin NV, Pankratov TA, Rakitin AL, Ivanova AA et al. Hydrolytic capabilities as a key to environmental success: chitinolytic and cellulolytic Acidobacteria from acidic sub-Arctic soils and boreal peatlands. Front Microbiol 2018; 9:2775 [View Article] [PubMed]
    [Google Scholar]
  22. Eichorst SA, Breznak JA, Schmidt TM. Isolation and characterization of soil bacteria that define Terriglobus gen. nov., in the phylum Acidobacteria. Appl Environ Microbiol 2007; 73:2708–2717 [View Article] [PubMed]
    [Google Scholar]
  23. Jiang Y-W, Wang J, Chen M-H, Lv Y-Y, Qiu L-H et al. Acidipila dinghuensis sp. nov., an acidobacterium isolated from forest soil. Int J Syst Evol Microbiol 2016; 66:76–83 [View Article] [PubMed]
    [Google Scholar]
  24. Myers MR, King GM. Isolation and characterization of Acidobacterium ailaaui sp. nov., a novel member of Acidobacteria subdivision 1, from a geothermally heated Hawaiian microbial mat. Int J Syst Evol Microbiol 2016; 66:5328–5335 [View Article] [PubMed]
    [Google Scholar]
  25. DeLong EF. Archaea in coastal marine environments. Proc Natl Acad Sci USA 1992; 89:5685–5689 [View Article] [PubMed]
    [Google Scholar]
  26. Lagesen K, Hallin P, Rødland EA, Staerfeldt H-H, Rognes T et al. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007; 35:3100–3108 [View Article] [PubMed]
    [Google Scholar]
  27. Yoon S-H, Ha S-M, 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]
  28. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article] [PubMed]
    [Google Scholar]
  29. 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]
  30. Fitch WM. Toward defining the course of evolution: minimum change for a specific tree topology. Systematic Biology 1971; 20:406–416 [View Article]
    [Google Scholar]
  31. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article] [PubMed]
    [Google Scholar]
  32. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16:111–120 [View Article] [PubMed]
    [Google Scholar]
  33. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article]
    [Google Scholar]
  34. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008; 18:821–829 [View Article] [PubMed]
    [Google Scholar]
  35. Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH et al. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res 2017; 27:722–736 [View Article] [PubMed]
    [Google Scholar]
  36. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article] [PubMed]
    [Google Scholar]
  37. Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010; 11:119 [View Article] [PubMed]
    [Google Scholar]
  38. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389–3402 [View Article] [PubMed]
    [Google Scholar]
  39. Tatusov RL, Galperin MY, Natale DA, Koonin EV. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 2000; 28:33–36 [View Article] [PubMed]
    [Google Scholar]
  40. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M et al. The KEGG resource for deciphering the genome. Nucleic Acids Res 2004; 32:D277–80 [View Article] [PubMed]
    [Google Scholar]
  41. Boeckmann B, Bairoch A, Apweiler R, Blatter M-C, Estreicher A et al. The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res 2003; 31:365–370 [View Article] [PubMed]
    [Google Scholar]
  42. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article] [PubMed]
    [Google Scholar]
  43. Lee I, Ouk Kim Y, Park S-C, Chun J. OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016; 66:1100–1103 [View Article] [PubMed]
    [Google Scholar]
  44. 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]
  45. Eichorst SA, Trojan D, Roux S, Herbold C, Rattei T et al. Genomic insights into the Acidobacteria reveal strategies for their success in terrestrial environments. Environ Microbiol 2018; 20:1041–1063 [View Article] [PubMed]
    [Google Scholar]
  46. Na S-I, Kim YO, Yoon S-H, Ha S-M, Baek I et al. UBCG: Up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 2018; 56:280–285 [View Article] [PubMed]
    [Google Scholar]
  47. Eddy SR. Accelerated profile HMM searches. PLoS Comput Biol 2011; 7:e1002195 [View Article] [PubMed]
    [Google Scholar]
  48. Price MN, Dehal PS, Arkin AP. FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article] [PubMed]
    [Google Scholar]
  49. Segata N, Börnigen D, Morgan XC, Huttenhower C. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat Commun 2013; 4:2304 [View Article] [PubMed]
    [Google Scholar]
  50. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article] [PubMed]
    [Google Scholar]
  51. Rawat SR, Männistö MK, Bromberg Y, Häggblom MM. Comparative genomic and physiological analysis provides insights into the role of Acidobacteria in organic carbon utilization in Arctic tundra soils. FEMS Microbiol Ecol 2012; 82:341–355 [View Article] [PubMed]
    [Google Scholar]
  52. Sait M, Hugenholtz P, Janssen PH. Cultivation of globally distributed soil bacteria from phylogenetic lineages previously only detected in cultivation-independent surveys. Environ Microbiol 2002; 4:654–666 [View Article] [PubMed]
    [Google Scholar]
  53. Buck JD. Nonstaining (KOH) method for determination of gram reactions of marine bacteria. Appl Environ Microbiol 1982; 44:992–993 [View Article] [PubMed]
    [Google Scholar]
  54. Miller LT. Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxy acids. J Clin Microbiol 1982; 16:584–586 [View Article] [PubMed]
    [Google Scholar]
  55. Kuykendall LD, Roy MA, O’neill JJ, Devine TE. Fatty acids, antibiotic resistance, and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum. Int J Syst Bacteriol 1988; 38:358–361 [View Article]
    [Google Scholar]
  56. Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M et al. An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 1984; 2:233–241 [View Article]
    [Google Scholar]
  57. Barco RA, Garrity GM, Scott JJ, Amend JP, Nealson KH et al. A genus definition for bacteria and archaea based on aa standard genome relatedness index. mBio 2020; 11: [View Article]
    [Google Scholar]
  58. Xu Z, Masuda Y, Wang X, Ushijima N, Shiratori Y et al. Genome-based taxonomic rearrangement of the order Geobacterales including the description of Geomonas azotofigens sp. nov. and Geomonas diazotrophica sp. nov. Front Microbiol 2021; 12:737531 [View Article]
    [Google Scholar]
  59. Parks DH, Chuvochina M, Chaumeil P-A, Rinke C, Mussig AJ et al. A complete domain-to-species taxonomy for Bacteria and Archaea. Nat Biotechnol 2020; 38:1079–1086 [View Article] [PubMed]
    [Google Scholar]
  60. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsl 1990; 20:1–6
    [Google Scholar]
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