Abstract
To better understand the taxonomy of Erwinia in the context of the Erwiniaceae family, we carried out a taxogenomic analysis of the Erwiniaceae, a family that was created following the taxonomic revision of the family, Enterobacteriaceae. There has been no systematic analysis of this family, including the agriculturally relevant genus, Erwinia. Our analyses focused on 80 strains of Erwinia along with 37 strains representing 7 other genera in the family. We identified 308 common proteins, generated a genome-level phylogeny and carried out Average Nucleotide Identity, Average Amino Acid Identity and Percentage of Conserved Protein analyses. We show that multiple strains of Erwinia cannot be assigned to established species groups and that both Erwinia gerundensis and “Erwinia mediterraneensis” are not members of Erwinia. We propose the creation of the genus Duffyella gen. nov. and the reclassification of Erwinia gerundensis to this genus as the type species, Duffyella gerundensis comb. nov. Furthermore, divergence between other species within Erwinia as measured by Average Amino Acid Identity is greater than the divergence between Erwinia and other genera, supporting the possible subdivision of the genus Erwinia into at least two genera. Our analyses also suggest that there is no basis for the establishment of the genus Kalamiella within the Erwiniaceae or the taxonomic revision of the Pantoea septica lineage. Therefore, we propose reclassifying Kalamiella piersonii as Pantoea piersonii comb. nov. Our study provides new insight into the diversity of the Erwiniaceae and provides a solid foundation for advancing taxonomic revision of this broadly relevant family.
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References
Adeolu M, Alnajar S, Naushad S, Gupta SRS (2016) Genome-based phylogeny and taxonomy of the “Enterobacteriales”: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol 66:5575–5599. https://doi.org/10.1099/ijsem.0.001485
Alnajar S, Gupta RS (2017) Phylogenomics and comparative genomic studies delineate six main clades within the family Enterobacteriaceae and support the reclassification of several polyphyletic members of the family. Infect Genet Evol 54:108–127. https://doi.org/10.1016/j.meegid.2017.06.024
Bergsten J (2005) A review of long-branch attraction. Cladistics 21:163–193. https://doi.org/10.1111/j.1096-0031.2005.00059.x
Bonnet I, Bozzi B, Fourniols E et al (2019) Erwinia billingiae as unusual cause of septic arthritis, France, 2017. Emerg Infect Dis 25:1587–1589
Brady C, Cleenwerck I, Venter S et al (2008) Phylogeny and identification of Pantoea species associated with plants, humans and the natural environment based on multilocus sequence analysis (MLSA). Syst Appl Microbiol 31:447–460. https://doi.org/10.1016/j.syapm.2008.09.004
Brady CL, Venter SN, Cleenwerck I et al (2010) Transfer of Pantoea citrea, Pantoea punctata and Pantoea terrea to the genus Tatumella emend. as Tatumella citrea comb. nov., Tatumella punctata comb. nov. and Tatumella terrea comb. nov. and description of Tatumella morbirosei sp. nov. Int J Syst Evol Microbiol 60:484–494. https://doi.org/10.1099/ijs.0.012070-0
Campillo T, Luna E, Portier P et al (2015) Erwinia iniecta sp. nov., isolated from Russian wheat aphid (Diuraphis noxia). Int J Syst Evol Microbiol 65:3625–3633. https://doi.org/10.1099/ijsem.0.000466
Capuzzo C, Firrao G, Mazzon L et al (2005) “Candidatus Erwinia dacicola”, a coevolved symbiotic bacterium of the olive fly Bactrocera oleae (Gmelin). Int J Syst Evol Microbiol 55:1641–1647. https://doi.org/10.1099/ijs.0.63653-0
Contreras-Moreira B, Vinuesa P (2013) GET_HOMOLOGUES, a versatile software package for scalable and robust microbial pangenome analysis. Appl Environ Microbiol 79:7696–7701. https://doi.org/10.1128/AEM.02411-13
Di D, Posada D, Kozlov AM et al (2020) ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Mol Biol Evol 37:291–294. https://doi.org/10.1093/molbev/msz189
Figueras MJ, Beaz-Hidalgo R, Hossain MJ, Liles MR (2014) Taxonomic affiliation of new genomes should be verified using average nucleotide identity and multilocus phylogenetic analysis. Genome Announc. https://doi.org/10.1128/genomeA.00927-14
Gao J-L, Xue J, Yan H et al (2019) Pantoea endophytica sp. nov., novel endophytic bacteria isolated from maize planting in different geographic regions of northern China. Syst Appl Microbiol 42:488–494. https://doi.org/10.1016/j.syapm.2019.06.001
Geider K, Auling G, Du Z et al (2006) Erwinia tasmaniensis sp. nov., a non-phytopathogenic bacterium from apple and pear trees. Int J Syst Evol Microbiol 56:2937–2943. https://doi.org/10.1099/ijs.0.64032-0
Goris J, Konstantinidis KT, Klappenbach JA et al (2007) DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91. https://doi.org/10.1099/ijs.0.64483-0
Gupta RS (2019) Distinction between Borrelia and Borreliella is more robustly supported by molecular and phenotypic characteristics than all other neighbouring prokaryotic genera: response to Margos’ et al. “The genus Borrelia reloaded” (PLoS ONE 13(12): e0208432). PLoS One. https://doi.org/10.1371/journal.pone.0221397
Harris et al (2017) Phylogenomics and comparative genomics of Lactobacillus salivarius, a mammalian gut commensal. Microb Genomics 3(8). https://doi.org/10.1099/mgen.0.000115
Huelsenbeck JP (1995) The robustness of two phylogenetic methods: four-taxon simulations reveal a slight superiority of maximum likelihood over neighbor joining. Mol Biol Evol 12:843–849. https://doi.org/10.1093/oxfordjournals.molbev.a040261
Imhoff JF (2005) Enterobacteriales. Bergey’s manual® of systematic bacteriology. Springer, Boston, pp 587–850
Jiang L, Wang D, Kim J-S et al (2020) Reclassification of genus Izhakiella into the family Erwiniaceae based on phylogenetic and genomic analyses. Int J Syst Evol Microbiol 70:3541–3546. https://doi.org/10.1099/ijsem.0.004192
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Konstantinidis KT, Tiedje JM (2005) Towards a genome-based taxonomy for prokaryotes. J Bacteriol 187:6258–6264. https://doi.org/10.1128/JB.187.18.6258-6264.2005
Kozlov AM, Darriba D, Flouri T et al (2019) RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35:4453–4455. https://doi.org/10.1093/bioinformatics/btz305
Kube M, Migdoll AM, Gehring I et al (2010) Genome comparison of the epiphytic bacteria Erwinia billingiae and E. tasmaniensis with the pear pathogen E. pyrifoliae. BMC Genomics. https://doi.org/10.1186/1471-2164-11-393
Kumar S, Stecher G, Li M et al (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Lalucat J, Mulet M, Gomila M, García-Valdés E (2020) Genomics in bacterial taxonomy: impact on the genus Pseudomonas. Genes (Basel). https://doi.org/10.3390/genes11020139
Luo C, Rodriguez-R LM, Konstantinidis KT (2014) MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences. Nucleic Acids Res. https://doi.org/10.1093/nar/gku169
Ma Y, Yao R, Li Y et al (2020) Proposal for unification of the genus Metakosakonia and the genus Phytobacter to a single genus Phytobacter and reclassification of Metakosakonia massiliensis as Phytobacter massiliensis comb. nov. Curr Microbiol 77:1945–1954. https://doi.org/10.1007/s00284-020-02004-4
Marchler-Bauer A, Bryant SH (2004) CD-search: protein domain annotations on the fly. Nucleic Acids Res. https://doi.org/10.1093/nar/gkh454
Marchler-Bauer A, Lu S, Anderson JB et al (2011) CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res. https://doi.org/10.1093/nar/gkq1189
Mateo-Estrada V, Graña-Miraglia L, López-Leal G et al (2019) Phylogenomics reveals clear cases of misclassification and genus-wide phylogenetic markers for Acinetobacter. Genome Biol Evol 11:2531–2541. https://doi.org/10.1093/gbe/evz178
Ndiaye C, Lo CI, Bassene H et al (2019) Lysinibacillus timonensis sp. nov., Microbacterium timonense sp. nov., and Erwinia mediterraneensis sp. nov., three new species isolated from the human skin. New Microbes New Infect. https://doi.org/10.1016/j.nmni.2019.100579
Oh CS, Beer SV (2005) Molecular genetics of Erwinia amylovora involved in the development of fire blight. FEMS Microbiol Lett 253:185–192. https://doi.org/10.1016/j.femsle.2005.09.051
Orata FD, Meier-Kolthoff JP, Sauvageau D, Stein LY (2018) Phylogenomic analysis of the gammaproteobacterial methanotrophs (order Methylococcales) calls for the reclassification of members at the genus and species levels. Front Microbiol. https://doi.org/10.3389/fmicb.2018.03162
Oren A, Garrity GM (2019) List of new names and new combinations that have appeared in effective publications outside of the IJSEM and are submitted for valid publication. Int J Syst Evol Microbiol 71:004688. https://doi.org/10.1099/ijsem.0.004688
Palmer M, Steenkamp ET, Coetzee MPA et al (2017) Phylogenomic resolution of the bacterial genus Pantoea and its relationship with Erwinia and Tatumella. Antonie Leeuwenhoek Int J Gen Mol Microbiol 110:1287–1309. https://doi.org/10.1007/s10482-017-0852-4
Palmer M, Steenkamp ET, Coetzee MPA et al (2018) Mixta gen. nov., a new genus in the Erwiniaceae. Int J Syst Evol Microbiol 68:1396–1407. https://doi.org/10.1099/ijsem.0.002540
Palmer M, Venter SN, McTaggart AR et al (2019) The synergistic effect of concatenation in phylogenomics: the case in Pantoea. PeerJ 7:e6698. https://doi.org/10.7717/peerj.6698
Pantiukh K, Grouzdev D (2017) POCP-matrix calculation for a number of genomes. Figshare. https://doi.org/10.6084/m9.figshare.5602957.v1
Parcey M, Gayder S, Morley-Senkler V et al (2020) Comparative genomic analysis of Erwinia amylovora reveals novel insights in phylogenetic arrangement, plasmid diversity, and streptomycin resistance. Genomics. https://doi.org/10.1016/j.ygeno.2020.04.001
Parks DH, Chuvochina M, Chaumeil PA et al (2020) A complete domain-to-species taxonomy for Bacteria and Archaea. Nat Biotechnol 38:1079–1086. https://doi.org/10.1038/s41587-020-0501-8
Parte AC (2014) LPSN–List of prokaryotic names with standing in nomenclature. Nucleic Acids Res. https://doi.org/10.1093/nar/gkt1111
Pritchard L, Glover RH, Humphris S et al (2016) Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Anal Methods 8:12–24
Prodhomme M, Micol LA, Weitsch S et al (2017) Cutaneous infection and bactaeremia caused by Erwinia billingiae: a case report. New Microbes New Infect 19:134–136
Qin QL, Bin XB, Zhang XY et al (2014) A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 196:2210–2215. https://doi.org/10.1128/JB.01688-14
Rezzonico F, Smits THM, Born Y et al (2016) Erwinia gerundensis sp. nov., a cosmopolitan epiphyte originally isolated from pome fruit trees. Int J Syst Evol Microbiol 66:1583–1592. https://doi.org/10.1099/ijsem.0.000920
Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131. https://doi.org/10.1073/pnas.0906412106
Rodriguez-R LM, Konstantinidis KT (2014) Bypassing cultivation to identify bacterial species. Microbe 9:111–118
Rodriguez-R L, Konstantinidis K (2016) The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ. https://doi.org/10.7287/peerj.preprints.1900
Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069. https://doi.org/10.1093/bioinformatics/btu153
Shapiro LR, Scully ED, Straub TJ et al (2016) Horizontal gene acquisitions, mobile element proliferation, and genome decay in the host-restricted plant pathogen Erwinia tracheiphila. Genome Biol Evol 8:649–664. https://doi.org/10.1093/gbe/evw016
Singh NK, Wood JM, Mhatre SS, Venkateswaran K (2019) Metagenome to phenome approach enables isolation and genomics characterization of Kalamiella piersonii gen. nov., sp. nov. from the International Space Station. Appl Microbiol Biotechnol 103:4483–4497. https://doi.org/10.1007/s00253-019-09813-z
Soutar CD, Stavrinides J (2019) Molecular validation of clinical Pantoea isolates identified by MALDI-TOF. PLoS One. https://doi.org/10.1371/journal.pone.0224731
Soutar CD, Stavrinides J (2020) Phylogenetic analysis supporting the taxonomic revision of eight genera within the bacterial order Enterobacterales. Int J Syst Evol Microbiol. https://doi.org/10.1099/ijsem.0.004542
Tambong JT (2019) Taxogenomics and systematics of the genus Pantoea. Front Microbiol 10:2463. https://doi.org/10.3389/fmicb.2019.02463
Thompson CC, Chimetto L, Edwards RA et al (2013) Microbial genomic taxonomy. BMC Genomics 14:913
Xia M, Wang J, Huo YX, Yang Y (2020) Mixta tenebrionis sp. Nov., isolated from the gut of the plastic-eating mealworm Tenebrio molitor L. Int J Syst Evol Microbiol 70:790–796. https://doi.org/10.1099/ijsem.0.003826
Zeng Q, Cui Z, Wang J et al (2018) Comparative genomics of Spiraeoideae-infecting Erwinia amylovora strains provides novel insight to genetic diversity and identifies the genetic basis of a low-virulence strain. Mol Plant Pathol 19:1652–1666. https://doi.org/10.1111/mpp.12647
Zhang Y, Qiu S (2015) Examining phylogenetic relationships of Erwinia and Pantoea species using whole genome sequence data. Antonie Leeuwenhoek Int J Gen Mol Microbiol 108:1037–1046. https://doi.org/10.1007/s10482-015-0556-6
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This work was supported by the Natural Sciences and Engineering Research Council of Canada (2015–06417).
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Soutar, C.D., Stavrinides, J. Phylogenomic analysis of the Erwiniaceae supports reclassification of Kalamiella piersonii to Pantoea piersonii comb. nov. and Erwinia gerundensis to the new genus Duffyella gen. nov. as Duffyella gerundensis comb. nov. Mol Genet Genomics 297, 213–225 (2022). https://doi.org/10.1007/s00438-021-01829-3
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DOI: https://doi.org/10.1007/s00438-021-01829-3