1887

Abstract

The members of the genus are key players in the removal of petroleum hydrocarbons from polluted marine environments. More than half of the species were described in the last decade using 16S rRNA gene phylogeny and genomic-based metrics. However, the 16S rRNA gene identity (<94 %) between some members of the genus suggested their imprecise taxonomic status. In this study, we examined the taxonomic positions of species using 16S rRNA phylogeny and further validated them using phylogenomic-related indexes such as digital DNA–DNA hybridization (dDDH), average nucleotide identity (ANI), average amino acid identity (AAI), percentage of conserved proteins (POCP) and comparative genomic studies. ANI and dDDH values confirmed that all the species were well described at the species level. The phylotaxogenomic analysis showed that species formed three clades. The inter-clade values of AAI and POCP were less than 70 %. The pan-genome evaluation depicted that the members shared 1223 core genes and its number increased drastically when analysed clade-wise. Therefore, these results necessitate the transfer of clade II and clade III members into gen. nov. and gen. nov., respectively, along with the emended description of the genus .

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.005672
2023-01-10
2024-05-14
Loading full text...

Full text loading...

References

  1. Melekhina EN, Belykh ES, Markarova MY, Taskaeva AA, Rasova EE et al. Soil microbiota and microarthropod communities in oil contaminated sites in the European Subarctic. Sci Rep 2021; 11:19620 [View Article] [PubMed]
    [Google Scholar]
  2. Kim S-H, Kim J-G, Jung M-Y, Kim S-J, Gwak J-H et al. Ketobacter alkanivorans gen. nov., sp. nov., an n-alkane-degrading bacterium isolated from seawater. Int J Syst Evol Microbiol 2018; 68:2258–2264 [View Article]
    [Google Scholar]
  3. Knobloch S, Daussin A, Jóhannsson R, Marteinsson V. Pelagibaculum spongiae gen. nov., sp. nov., isolated from a marine sponge in South-West Iceland. Int J Syst Evol Microbiol 2019; 69:2129–2134 [View Article]
    [Google Scholar]
  4. Cappello S, Yakimov MM. Alcanivorax. In Timmis KN. eds Handbook of Hydrocarbon and Lipid Microbiology Berlin, Heidelberg: Springer; 2010 https://doi.org/10.1007/978-3-540-77587-4_123
    [Google Scholar]
  5. Yakimov MM, Golyshin PN, Lang S, Moore ER, Abraham WR et al. Alcanivorax borkumensis gen. nov., sp. nov., a new, hydrocarbon-degrading and surfactant-producing marine bacterium. Int J Syst Bacteriol 1998; 48 Pt 2:339–348 [View Article]
    [Google Scholar]
  6. Liu C, Shao Z. Alcanivorax dieselolei sp. nov., a novel alkane-degrading bacterium isolated from sea water and deep-sea sediment. Int J Syst Evol Microbiol 2005; 55:1181–1186 [View Article] [PubMed]
    [Google Scholar]
  7. Wu Y, Lai Q, Zhou Z, Qiao N, Liu C et al. Alcanivorax hongdengensis sp. nov., an alkane-degrading bacterium isolated from surface seawater of the straits of Malacca and Singapore, producing a lipopeptide as its biosurfactant. Int J Syst Evol Microbiol 2009; 59:1474–1479 [View Article] [PubMed]
    [Google Scholar]
  8. Song L, Liu H, Cai S, Huang Y, Dai X et al. Alcanivorax indicus sp. nov., isolated from seawater. Int J Syst Evol Microbiol 2018; 68:3785–3789 [View Article] [PubMed]
    [Google Scholar]
  9. Lai Q, Wang J, Gu L, Zheng T, Shao Z. Alcanivorax marinus sp. nov., isolated from deep-sea water. Int J Syst Evol Microbiol 2013; 63:4428–4432 [View Article] [PubMed]
    [Google Scholar]
  10. Liu J, Ren Q, Zhang Y, Li Y, Tian X et al. Alcanivorax profundi sp. nov., isolated from deep seawater of the Mariana Trench. Int J Syst Evol Microbiol 2019; 69:371–376 [View Article] [PubMed]
    [Google Scholar]
  11. Kyoung Kwon K, Hye Oh J, Yang S-H, Seo H-S, Lee J-H. Alcanivorax gelatiniphagus sp. nov., a marine bacterium isolated from tidal flat sediments enriched with crude oil. Int J Syst Evol Microbiol 2015; 65:2204–2208 [View Article] [PubMed]
    [Google Scholar]
  12. Fernández-Martínez J, Pujalte MJ, García-Martínez J, Mata M, Garay E et al. Description of Alcanivorax venustensis sp. nov. and reclassification of Fundibacter jadensis DSM 1 21 78T (Bruns and Berthe-Corti 1999) as Alcanivorax jadensis comb. nov., members of the emended genus Alcanivorax. Int J Syst Evol Microbiol 2003; 53:331–338 [View Article] [PubMed]
    [Google Scholar]
  13. Lai Q, Zhou Z, Li G, Li G, Shao Z. Alcanivorax nanhaiticus sp. nov., isolated from deep sea sediment. Int J Syst Evol Microbiol 2016; 66:3651–3655 [View Article] [PubMed]
    [Google Scholar]
  14. Lai Q, Wang L, Liu Y, Fu Y, Zhong H et al. Alcanivorax pacificus sp. nov., isolated from a deep-sea pyrene-degrading consortium. Int J Syst Evol Microbiol 2011; 61:1370–1374 [View Article] [PubMed]
    [Google Scholar]
  15. Dong C, Lai Q, Liu X, Gu L, Zhang Y et al. Alcanivorax profundimaris sp. nov., a novel marine hydrocarbonoclastic bacterium isolated from seawater and deep-sea sediment. Curr Microbiol 2021; 78:1053–1060 [View Article] [PubMed]
    [Google Scholar]
  16. Rivas R, García-Fraile P, Peix A, Mateos PF, Martínez-Molina E et al. Alcanivorax balearicus sp. nov., isolated from Lake Martel. Int J Syst Evol Microbiol 2007; 57:1331–1335 [View Article] [PubMed]
    [Google Scholar]
  17. Rahul K, Sasikala C, Tushar L, Debadrita R, Ramana CV. Alcanivorax xenomutans sp. nov., a hydrocarbonoclastic bacterium isolated from a shrimp cultivation pond. Int J Syst Evol Microbiol 2014; 64:3553–3558 [View Article] [PubMed]
    [Google Scholar]
  18. Olm MR, Crits-Christoph A, Diamond S, Lavy A, Matheus Carnevali PB et al. Consistent metagenome-derived metrics verify and delineate bacterial species boundaries. mSystems 2020; 5:e00731-19 [View Article] [PubMed]
    [Google Scholar]
  19. 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]
  20. Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the genome taxonomy database. Bioinformatics 2019; 36:1925–1927 [View Article] [PubMed]
    [Google Scholar]
  21. Salvetti E, Harris HMB, Felis GE, O’Toole PW. Comparative genomics of the genus Lactobacillus reveals robust phylogroups that provide the basis for reclassification. Appl Environ Microbiol 2018; 84:e00993-18 [View Article] [PubMed]
    [Google Scholar]
  22. Zheng J, Wittouck S, Salvetti E, Franz CMAP, Harris HMB et al. A taxonomic note on the genus Lactobacillus: description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int J Syst Evol Microbiol 2020; 70:2782–2858 [View Article] [PubMed]
    [Google Scholar]
  23. Xu Z, Masuda Y, Itoh H, Ushijima N, Shiratori Y et al. Geomonas oryzae gen. nov., sp. nov., Geomonas edaphica sp. nov., Geomonas ferrireducens sp. nov., Geomonas terrae sp. nov., four ferric-reducing bacteria isolated from paddy soil, and reclassification of three species of the genus Geobacter as members of the genus Geomonas gen. nov. Front Microbiol 2019; 10: [View Article]
    [Google Scholar]
  24. Green PN, Ardley JK. Review of the genus Methylobacterium and closely related organisms: a proposal that some Methylobacterium species be reclassified into a new genus, Methylorubrum gen. nov. Int J Syst Evol Microbiol 2018; 68:2727–2748 [View Article] [PubMed]
    [Google Scholar]
  25. Suresh G, Lodha TD, Indu B, Sasikala C, Ramana CV. Taxogenomics resolves conflict in the genus Rhodobacter: a two and half decades pending thought to reclassify the genus Rhodobacter. Front Microbiol 2019; 10:2480 [View Article] [PubMed]
    [Google Scholar]
  26. Rai A, Jagadeeshwari U, Deepshikha G, Smita N, Sasikala C et al. Phylotaxogenomics for the reappraisal of the genus Roseomonas with the creation of six new genera. Front Microbiol 2021; 12:12–677842 [View Article] [PubMed]
    [Google Scholar]
  27. Wirth JS, Whitman WB. Phylogenomic analyses of a clade within the Roseobacter group suggest taxonomic reassignments of species of the genera Aestuariivita, Citreicella, Loktanella, Nautella, Pelagibaca, Ruegeria, Thalassobius, Thiobacimonas and Tropicibacter, and the proposal of six novel genera. Int J Syst Evol Microbiol 2018; 68:2393–2411 [View Article] [PubMed]
    [Google Scholar]
  28. Orata FD, Meier-Kolthoff JP, Sauvageau D, Stein LY. Phylogenomic analysis of the gammaproteobacterial methanotrophs (order Methylococcales) calls for the reclassification of members at the genus and species levels. Front Microbiol 2018; 9:3162 [View Article] [PubMed]
    [Google Scholar]
  29. Hördt A, López MG, Meier-Kolthoff JP, Schleuning M, Weinhold L-M et al. Analysis of 1,000+ type-strain genomes substantially improves taxonomic classification of Alphaproteobacteria. Front Microbiol 2020; 11:468 [View Article] [PubMed]
    [Google Scholar]
  30. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
    [Google Scholar]
  31. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 2004; 32:1792–1797 [View Article]
    [Google Scholar]
  32. 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]
  33. 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]
  34. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article] [PubMed]
    [Google Scholar]
  35. Na S-I, Kim YO, Yoon S-H, Ha S, 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]
    [Google Scholar]
  36. Yoon SH, Ha SM, Lim JM, Kwon SJ, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article]
    [Google Scholar]
  37. Auch AF, Klenk HP, Göker M. Standard operating procedure for calculating genome-to-genome distances based on high-scoring segment pairs. Stand Genomic Sci 2010; 2:142–148 [View Article]
    [Google Scholar]
  38. Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Preprints 2016; 4: [View Article]
    [Google Scholar]
  39. 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]
    [Google Scholar]
  40. Danielsson P-E. Euclidean distance mapping. Comput Graph 1980; 14:227–248 [View Article]
    [Google Scholar]
  41. Chaudhari NM, Gupta VK, Dutta C. BPGA- an ultra-fast pan-genome analysis pipeline. Sci Rep 2016; 6:24373 [View Article] [PubMed]
    [Google Scholar]
  42. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010; 26:2460–2461 [View Article] [PubMed]
    [Google Scholar]
  43. Blin K, Shaw S, Steinke K, Villebro R, Ziemert N et al. antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 2019; 47:W81–W87 [View Article]
    [Google Scholar]
  44. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST Server: Rapid Annotations using Subsystems Technology. BMC Genomics 2008; 9:9–75 [View Article]
    [Google Scholar]
  45. Davis JJ, Wattam AR, Aziz RK, Brettin T, Butler R et al. The PATRIC Bioinformatics Resource Center: expanding data and analysis capabilities. Nucleic acids Res 2020; 48:606–612 [View Article]
    [Google Scholar]
  46. Golyshin PN, Harayama S, Timmis KN, Yakimov MM. Family II. Alcanivoraceae fam. nov. In Brenner DJ, Krieg NR, Staley JT, Garrity GM. eds Bergey’s Manual of Systematic Bacteriology, 2nd. edn vol 2 New York: Springer; 2005 p 295
    [Google Scholar]
  47. Tindall BJ, Rosselló-Móra R, Busse H-J, Ludwig W, Kämpfer P. Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 2010; 60:249–266 [View Article] [PubMed]
    [Google Scholar]
  48. 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 [View Article] [PubMed]
    [Google Scholar]
  49. Chernikova TN, Bargiela R, Toshchakov SV, Shivaraman V, Lunev EA et al. Hydrocarbon-degrading bacteria Alcanivorax and Marinobacter associated with microalgae Pavlova lutheri and Nannochloropsis oculata. Front Microbiol 2020; 11:572931 [View Article]
    [Google Scholar]
  50. Chun J, Rainey FA. Integrating genomics into the taxonomy and systematics of the Bacteria and Archaea. Int J Syst Evol Microbiol 2014; 64:316–324 [View Article] [PubMed]
    [Google Scholar]
  51. 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]
  52. Wayne LG, Brenner DJ, Colwell RR, Grimont P AD, Kandler O et al. International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 1984; 37:463–464 [View Article]
    [Google Scholar]
  53. 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]
  54. Rodriguez-R LM, Konstantinidis KT. Bypassing cultivation to identify bacterial species. Microbe Magazine 2014; 9:111–118 [View Article]
    [Google Scholar]
  55. Rosselló-Móra R, Amann R. Past and future species definitions for bacteria and archaea. Syst Appl Microbiol 2015; 38:209–216 [View Article] [PubMed]
    [Google Scholar]
  56. Nouioui I, Carro L, García-López M, Meier-Kolthoff JP, Woyke T et al. Genome-based taxonomic classification of the phylum Actinobacteria. Front Microbiol 2018; 9:2007 [View Article] [PubMed]
    [Google Scholar]
  57. Luo C, Rodriguez-R LM, Konstantinidis KT. MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences. Nucleic Acids Res 2014; 42:e73 [View Article] [PubMed]
    [Google Scholar]
  58. Liu A, Zhang Y-J, Cheng P, Peng Y-J, Blom J et al. Whole genome analysis calls for a taxonomic rearrangement of the genus Colwellia. Antonie van Leeuwenhoek 2020; 113:919–931 [View Article] [PubMed]
    [Google Scholar]
  59. Rojo F. Degradation of alkanes by bacteria. Environ Microbiol 2009; 11:2477–2490 [View Article]
    [Google Scholar]
  60. Garrity GM. A new genomics-driven taxonomy of bacteria and archaea: are we there yet?. J Clin Microbiol 2016; 54:1956–1963 [View Article] [PubMed]
    [Google Scholar]
  61. Yang S, Li M, Lai Q, Li G, Shao Z. Alcanivorax mobilis sp. nov., a new hydrocarbon-degrading bacterium isolated from deep-sea sediment. Int J Syst Evol Microbiol 2018; 68:1639–1643 [View Article] [PubMed]
    [Google Scholar]
  62. Bruns A, Berthe-Corti L. Fundibacter jadensis gen. nov., sp. nov., a new slightly halophilic bacterium, isolated from intertidal sediment. Int J Syst Bacteriol 1999; 49 Pt 2:441–448 [View Article] [PubMed]
    [Google Scholar]
  63. Liao X, Lai Q, Yang J, Dong C, Li D et al. Alcanivorax sediminis sp. nov., isolated from deep-sea sediment of the Pacific Ocean. Int J Syst Evol Microbiol 2020; 70:4280–4284 [View Article] [PubMed]
    [Google Scholar]
  64. Li J, Qi M, Lai Q, Liu X, Shao Z. Ketobacter nezhaii sp. nov., a marine bacterium isolated from coastal sediment. Int J Syst Evol Microbiol 2020; 70:4960–4965 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.005672
Loading
/content/journal/ijsem/10.1099/ijsem.0.005672
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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