1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 73, Issue 11

Phylotaxonomic assessment based on four core gene sets and proposal of a genus definition among the families and No Access

Abstract

The families and comprise metabolically, phenotypically and genotypically diverse members, and their descriptions rely heavily on 16S rRNA gene analysis. Hundreds of genera have been reported within the two families and misclassifications have been a reoccurring problem, even when the taxonomies have been established based on genome-scale phylogenetic reconstructions. In this study, we conducted a comprehensive phylotaxonomic assessment of the families and based on four ubiquitous gene sets, bac120 (120 genes in Bacteria), rhodo268 (268 genes in ‘’, defined in this study), rp1 (16 ribosomal protein genes in Prokaryote) and rp2 (23 ribosomal protein genes in Prokaryote), using two tree-inferring applications and two approaches (supermatrix and consensus). The results suggested that the four supermatrix trees based on bac120 and rhodo268 shared a high proportion of common nodes (>88.4 %) and the topology was reproducible among all the trees within most of the genera. The evolutionary distance (ED) analysis showed significant overlapping between the intergeneric and intrageneric comparisons, implying that the proposal of some genera seemed to be unnecessary. In addition, the bac120 gene set and the FastTree program were found to be the most cost-effective way to conduct phylogenomic analysis of the families and . An ED threshold of 0.21–0.23 based on either bac120 or rhodo268 was proposed as one standard for later genus delimitation in these families. A comprehensive phylogenetic framework is presented in this study and the proposed genus definition will help to establish a more reasonable taxonomy in the families and .

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): EasyCGTree , Paracoccaceae , phylogenomic tree , Rhodobacteraceae and Roseobacteraceae
Funding
This study was supported by the:
  • Postdoctoral Research Foundation of China (Award 2020M671312)
    • Principle Award Recipient: Dao-FengZhang
  • Innovation Project for Marine Science and Technology of Jiangsu Province (Award JSZRHYKJ202209)
    • Principle Award Recipient: Dao-FengZhang
  • Young Scientists Fund (Award 31900001)
    • Principle Award Recipient: Dao-FengZhang
© 2023 The Authors

Erratum

An erratum has been published for this content:
Corrigendum: Phylotaxonomic assessment based on four core gene sets and proposal of a genus definition among the families and
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.006156
2023-11-16
2024-05-03
Loading full text...

Full text loading...

References

  1. Zhang D-F, He W, Shao Z, Ahmed I, Zhang Y et al.Phylotaxonomic assessment based on four core gene sets and proposal of a genus definition among the families Paracoccaceae and Roseobacteraceae Figshare 2023 [View Article]
     [Google Scholar]
  2. Snel B, Huynen MA, Dutilh BE. Genome trees and the nature of genome evolution. Annu Rev Microbiol 2005; 59:191–209 [View Article] [PubMed]
     [Google Scholar]
  3. Hugenholtz P, Chuvochina M, Oren A, Parks DH, Soo RM. Prokaryotic taxonomy and nomenclature in the age of big sequence data. ISME J 2021; 15:1879–1892 [View Article] [PubMed]
     [Google Scholar]
  4. McInerney JO, Cotton JA, Pisani D. The prokaryotic tree of life: past, present and future?. Trends Ecol Evol 2008; 23:276–281 [View Article] [PubMed]
     [Google Scholar]
  5. Pisani D, Wilkinson M. Matrix representation with parsimony, taxonomic congruence, and total evidence. Syst Biol 2002; 51:151–155 [View Article] [PubMed]
     [Google Scholar]
  6. Tümmler B. Molecular epidemiology in current times. Environ Microbiol 2020; 22:4909–4918 [View Article] [PubMed]
     [Google Scholar]
  7. Jolley KA, Bliss CM, Bennett JS, Bratcher HB, Brehony C et al. Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain. Microbiology 2012; 158:1005–1015 [View Article] [PubMed]
     [Google Scholar]
  8. 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]
  9. 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]
  10. Garrity GM, Bell JA, Lilburn T et al. Rhodobacteraceae fam. nov. In Trujillo ME, Dedysh S, DeVos P, Hedlund B, Kämpfer P et al. eds Bergey’s Manual of Systematics of Archaea Bacteria Hoboken, NJ: John Wiley & Sons, Inc; 2015 [View Article]
     [Google Scholar]
  11. 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]
  12. Zhang S, Liu W-X, Liu N-H, He X-Y, Su H-N et al. Antarcticimicrobium sediminis gen. nov., sp. nov., isolated from Antarctic intertidal sediment, transfer of Ruegeria lutea to Antarcticimicrobium gen. nov. as Antarcticimicrobium luteum comb. nov. Int J Syst Evol Microbiol 2020; 70:2624–2631 [View Article] [PubMed]
     [Google Scholar]
  13. Liu Y, Pei T, Du J, Chao M, Deng M-R et al. Roseibium litorale sp. nov., isolated from a tidal flat sediment and proposal for the reclassification of Labrenzia polysiphoniae as Roseibium polysiphoniae comb. nov. Int J Syst Evol Microbiol 2021; 71: [View Article] [PubMed]
     [Google Scholar]
  14. Liang KYH, Orata FD, Boucher YF, Case RJ. Roseobacters in a sea of poly- and paraphyly: whole genome-based taxonomy of the family Rhodobacteraceae and the proposal for the split of the “Roseobacter clade” into a novel family, Roseobacteraceae fam. nov. Front Microbiol 2021; 12:683109 [View Article] [PubMed]
     [Google Scholar]
  15. Wang YW, Ren WT, Xu YY, Zhang XQ. Muriiphilus fusiformis gen. nov., sp. nov., a novel non-marine bacterium belonging to the Roseobacter group, and reclassification of Maritimibacter lacisalsi. Int J Syst Evol Microbiol 2021; 71:004859 [View Article] [PubMed]
     [Google Scholar]
  16. Xu L, Liu A, Zhang YJ. Zongyanglinia huanghaiensis gen. nov., sp. nov., a novel denitrifying bacterium isolated from the yellow sea, and transfer of Pelagicola marinus to Zongyanglinia gen. nov. as Zongyanglinia marinus comb. nov. Antonie van Leeuwenhoek 2021; 114:137–149 [View Article] [PubMed]
     [Google Scholar]
  17. Ma T, Xue H, Piao C, Liu C, Yang M et al. Reclassification of 11 members of the family Rhodobacteraceae at genus and species levels and proposal of Pseudogemmobacter hezensis sp. nov. Front Microbiol 2022; 13:849695 [View Article] [PubMed]
     [Google Scholar]
  18. Qu L, Li Y, Wang W, Shao Z, Gao Z et al. Aestuarium zhoushanense is a later heterotypic synonym of Marivivens donghaensis, and transfer of Paradonghicola geojensis to the genus Marivivens as Marivivens geojensis comb. nov. Int J Syst Evol Microbiol 2022; 72:11 [View Article]
     [Google Scholar]
  19. 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]
  20. Göker M. Filling the gaps: missing taxon names at the ranks of class, order and family. Int J Syst Evol Microbiol 2022; 72:12 [View Article]
     [Google Scholar]
  21. Simon M, Scheuner C, Meier-Kolthoff JP, Brinkhoff T, Wagner-Döbler I et al. Phylogenomics of Rhodobacteraceae reveals evolutionary adaptation to marine and non-marine habitats. ISME J 2017; 11:1483–1499 [View Article] [PubMed]
     [Google Scholar]
  22. Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M. List of Prokaryotic names with Standing in Nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 2020; 70:5607–5612 [View Article] [PubMed]
     [Google Scholar]
  23. Li CM, Wang XP, Zhou LY, Chen GJ, Du ZJ. Pelagivirga dicentrarchi sp. nov., a member of the family Rhodobacteraceae isolated from the gut microflora of sea bass (Dicentrarchus labrax L.). Antonie van Leeuwenhoek 2020; 113:293–301 [View Article] [PubMed]
     [Google Scholar]
  24. Hameed A, Shahina M, Lin S-Y, Chen W-M, Hsu Y-H et al. Description of Gemmobacter aestuarii sp. nov., isolated from estuarine surface water and reclassification of Cereibacter changlensis as Gemmobacter changlensis Chen et al. 2013. Arch Microbiol 2020; 202:1035–1042 [View Article] [PubMed]
     [Google Scholar]
  25. Barnier C, Clerissi C, Lami R, Intertaglia L, Lebaron P et al. Description of Palleronia rufa sp. nov., a biofilm-forming and AHL-producing Rhodobacteraceae, reclassification of Hwanghaeicola aestuarii as Palleronia aestuarii comb. nov., Maribius pontilimi as Palleronia pontilimi comb. nov., Maribius salinus as Palleronia salina comb. nov., Maribius pelagius as Palleronia pelagia comb. nov. and emended description of the genus Palleronia. Syst Appl Microbiol 2020; 43:126018 [View Article] [PubMed]
     [Google Scholar]
  26. Parks DH, Rinke C, Chuvochina M, Chaumeil P-A, Woodcroft BJ et al. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat Microbiol 2017; 2:1533–1542 [View Article] [PubMed]
     [Google Scholar]
  27. Brown CT, Hug LA, Thomas BC, Sharon I, Castelle CJ et al. Unusual biology across a group comprising more than 15% of domain bacteria. Nature 2015; 523:208–211 [View Article] [PubMed]
     [Google Scholar]
  28. Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 2013; 499:431–437 [View Article] [PubMed]
     [Google Scholar]
  29. Li W, O’Neill KR, Haft DH, DiCuccio M, Chetvernin V et al. RefSeq: expanding the prokaryotic genome annotation pipeline reach with protein family model curation. Nucleic Acids Res 2021; 49:D1020–D1028 [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. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 1991; 173:697–703 [View Article] [PubMed]
     [Google Scholar]
  32. Okonechnikov K, Golosova O, Fursov M. the UGENE team Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics 2012; 28:1166–1167 [View Article]
     [Google Scholar]
  33. Nurk S, Bankevich A, Antipov D, Gurevich AA, Korobeynikov A et al. Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J Comput Biol 2013; 20:714–737 [View Article] [PubMed]
     [Google Scholar]
  34. 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]
  35. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009; 106:19126–19131 [View Article] [PubMed]
     [Google Scholar]
  36. Zhao Y, Wu J, Yang J, Sun S, Xiao J et al. PGAP: pan-genomes analysis pipeline. Bioinformatics 2012; 28:416–418 [View Article] [PubMed]
     [Google Scholar]
  37. Zhang D-F, He W, Shao Z, Ahmed I, Zhang Y et al. EasyCGTree: a pipeline for prokaryotic phylogenomic analysis based on core gene sets. BMC Bioinformatics 2023; 24:390 [View Article] [PubMed]
     [Google Scholar]
  38. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011; 7:539 [View Article] [PubMed]
     [Google Scholar]
  39. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009; 25:1972–1973 [View Article] [PubMed]
     [Google Scholar]
  40. Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 2009; 26:1641–1650 [View Article] [PubMed]
     [Google Scholar]
  41. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 2020; 37:1530–1534 [View Article] [PubMed]
     [Google Scholar]
  42. Revell LJ, Chamberlain SA. Rphylip: an R interface for PHYLIP. Methods Ecol Evol 2014; 5:976–981 [View Article]
     [Google Scholar]
  43. Galili T. dendextend: an R package for visualizing, adjusting and comparing trees of hierarchical clustering. Bioinformatics 2015; 31:3718–3720 [View Article] [PubMed]
     [Google Scholar]
  44. Chen T, Liu Y-X, Huang L. ImageGP: an easy‐to‐use data visualization web server for scientific researchers. iMeta 2022; 1: [View Article]
     [Google Scholar]
  45. Kloepper TH, Huson DH. Drawing explicit phylogenetic networks and their integration into splitstree. BMC Evol Biol 2008; 8:22 [View Article] [PubMed]
     [Google Scholar]
  46. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article] [PubMed]
     [Google Scholar]
  47. Chu J-N, Arun AB, Chen W-M, Chou J-H, Shen F-T et al. Agaricicola taiwanensis gen. nov., sp. nov., an alphaproteobacterium isolated from the edible mushroom Agaricus blazei. Int J Syst Evol Microbiol 2010; 60:2032–2035 [View Article] [PubMed]
     [Google Scholar]
  48. Cai M, Wang L, Cai H, Li Y, Tang Y-Q et al. Rubrimonas shengliensis sp. nov. and Polymorphum gilvum gen. nov., sp. nov., novel members of Alphaproteobacteria from crude oil contaminated saline soil. Syst Appl Microbiol 2011; 34:321–327 [View Article] [PubMed]
     [Google Scholar]
  49. Kim YG, Hwang CY, Cho BC. Pelagicola litoralis gen. nov., sp. nov., isolated from coastal water in Korea. Int J Syst Evol Microbiol 2008; 58:2102–2106 [View Article] [PubMed]
     [Google Scholar]
  50. Doronina NV, Trotsenko YA, Tourova TP. Methylarcula marina gen. nov., sp. nov. and Methylarcula terricola sp. nov.: novel aerobic, moderately halophilic, facultatively methylotrophic bacteria from coastal saline environments. Int J Syst Evol Microbiol 2000; 50 Pt 5:1849–1859 [View Article] [PubMed]
     [Google Scholar]
  51. Nogi Y, Nishi S, Koyama S. Planktotalea lamellibrachiae sp. nov., isolated from a marine organism in Kagoshima Bay, Japan. Int J Syst Evol Microbiol 2017; 67:4785–4789 [View Article] [PubMed]
     [Google Scholar]
  52. Park S, Won SM, Yoon J-H. Paenimaribius caenipelagi gen. nov., sp. nov., isolated from a tidal flat. Int J Syst Evol Microbiol 2019; 69:3049–3055 [View Article] [PubMed]
     [Google Scholar]
  53. Hameed A, Shahina M, Lin S-Y, Nakayan P, Liu Y-C et al. Youngimonas vesicularis gen. nov., sp. nov., of the family Rhodobacteraceae, isolated from surface seawater, reclassification of Donghicola xiamenensis Tan et al. 2009 as Pseudodonghicola xiamenensis gen. nov., comb. nov. and emended description of the genus Donghicola Yoon et al. 2007. Int J Syst Evol Microbiol 2014; 64:2729–2737 [View Article] [PubMed]
     [Google Scholar]
  54. Zhang YJ, Yu N, Zhang XY, Chen S. Pseudopuniceibacterium sediminis gen. nov., sp. nov., a member of the family Rhodobacteraceae isolated from sediment. Int J Syst Evol Microbiol 2019; 69:2541–2546 [View Article] [PubMed]
     [Google Scholar]
  55. Liao L, Su S-Y, Zhang Y-J, Liu H, Zhang X-Y et al. Pseudopuniceibacterium antarcticum sp. nov., isolated from an Antarctic marine sponge. Int J Syst Evol Microbiol 2021; 71: [View Article] [PubMed]
     [Google Scholar]
  56. Rosselló-Mora R, Amann R. The species concept for prokaryotes. FEMS Microbiol Rev 2001; 25:39–67 [View Article] [PubMed]
     [Google Scholar]
  57. Kim D, Park S, Chun J. Introducing EzAAI: a pipeline for high throughput calculations of prokaryotic average amino acid identity. J Microbiol 2021; 59:476–480 [View Article] [PubMed]
     [Google Scholar]
  58. 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]
  59. 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]
  60. Barco RA, Garrity GM, Scott JJ, Amend JP, Nealson KH et al. A genus definition for bacteria and Archaea based on a standard genome relatedness index. mBio 2020; 11:e02475–02419
     [Google Scholar]
  61. Xu L, Sun C, Fang C, Oren A, Xu XW. Genomic-based taxonomic classification of the family Erythrobacteraceae. Int J Syst Evol Microbiol 2020; 70:4470–4495 [View Article] [PubMed]
     [Google Scholar]
  62. Xue H-P, Zhang D-F, Xu L, Wang X-N, Zhang A-H et al. Actirhodobacter atriluteus gen. nov., sp. nov., isolated from the surface water of the Yellow Sea. Antonie van Leeuwenhoek 2021; 114:1059–1068 [View Article] [PubMed]
     [Google Scholar]
  63. Sun J, Guo J, Lin T-H, Feng X, Zhang R. Pseudopontixanthobacter vadosimaris gen. nov., sp. nov., isolated from shallow sea near Kueishan Island. Int J Syst Evol Microbiol 2020; 70:6444–6449 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.006156
Loading
Phylotaxonomic assessment based on four core gene sets and proposal of a genus definition among the families Paracoccaceae and Roseobacteraceae
Int J Syst Evol Microbiol 73, 006156 (2023); https://doi.org/10.1099/ijsem.0.006156
/content/journal/ijsem/10.1099/ijsem.0.006156
/content/journal/ijsem/10.1099/ijsem.0.006156
Loading

Data & Media loading...

Supplements

Loading data from figshare Loading data from figshare

Most cited Most Cited RSS feed

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