Revisiting the Taxonomy of the Genus Arcobacter: Getting Order From the Chaos

Abstract

Since the description of the genus Arcobacter in 1991, a total of 27 species have been described, although some species have shown 16S rRNA similarities below 95%, which is the cut-off that usually separates species that belong to different genera. The objective of the present study was to reassess the taxonomy of the genus Arcobacter using information derived from the core genome (286 genes), a Multilocus Sequence Analysis (MLSA) with 13 housekeeping genes, as well as different genomic indexes like Average Nucleotide Identity (ANI), in silico DNA-DNA hybridization (isDDH), Average Amino-acid Identity (AAI), Percentage of Conserved Proteins (POCPs), and Relative Synonymous Codon Usage (RSCU). The study included a total of 39 strains that represent all the 27 species included in the genus Arcobacter together with 13 strains that are potentially new species, and the analysis of 57 genomes. The different phylogenetic analyses showed that the Arcobacter species grouped into four clusters. In addition, A. lekithochrous and the candidatus species 'A. aquaticus' appeared, as did A. nitrofigilis, the type species of the genus, in separate branches. Furthermore, the genomic indices ANI and isDDH not only confirmed that all the species were well-defined, but also the coherence of the clusters. The AAI and POCP values showed intra-cluster ranges above the respective cut-off values of 60% and 50% described for species belonging to the same genus. Phenotypic analysis showed that certain test combinations could allow the differentiation of the four clusters and the three orphan species established by the phylogenetic and genomic analyses. The origin of the strains showed that each of the clusters embraced species recovered from a common or related environment. The results obtained enable the division of the current genus Arcobacter in at least seven different genera, for which the names Arcobacter, Aliiarcobacter gen. nov., Pseudoarcobacter gen. nov., Haloarcobacter gen. nov., Malacobacter gen. nov., Poseidonibacter gen. nov., and Candidate 'Arcomarinus' gen. nov. are proposed.

Keywords: Aliiarcobacter gen. nov.; Arcobacter; Haloarcobacter gen. nov.; Malacobacter gen. nov.; Poseidonibacter gen. nov.; Pseudoarcobacter gen. nov.; taxonomic criteria.

FIGURE 1

Split decomposition network constructed with the concatenated sequences of 284 core genes from the genomes of 36 type and representative strains of Arcobacter. Scale bar, base substitutions per site.

FIGURE 2

Phylogenetic tree constructed with 36 type and representative strains of Arcobacter species based on concatenated sequences of 13 housekeeping genes by the Maximum-Likelihood algorithm (model GTR+G+I). Numbers at nodes denote the level of bootstrap based on 1,000 replicates; only values greater than 50% are shown. Scale bar, base substitutions per site.

FIGURE 3

3D plot of the three major axes generated by principal component analysis (PCA) of the RSCU values computed for the 36 type and representative strains of Arcobacter species. 1, A. anaerophilus DSM 24636^T; 2, ‘A. aquaticus’ W112-28; 3, A. aquimarinus CECT 8442^T; 4, A. bivalviorum; 5, A. butzleri RM4018^T; 6, ‘A. caeni’ RW17-10; 7, A. canalis CECT 8984^T; 8 A. cibarius LMG 21996^T; 9, A. cloacae CECT 7834^T; 10, A. cryaerophilus LMG 24291^T; 11, A. defluvii CECT 7697^T; 12, A. ebronensis F128-2^T; 13, A. ellisii CECT 7837^T; 14, A. faecis AF1078^T; 15, A. halophilus DSM 18005^T; 16, ‘A. hispanicus’ FW54; 17, ‘A. lacus’ RW43-9; 18, A. lanthieri AF1440^T; 19, A. lekithochrous LFT1.7^T; 20, A. marinus CECT 7727^T; 21, ‘A. mediterraneus’ F156-34; 22, ‘A. miroungae’ 9Ant; 23, A. molluscorum CECT 7696^T; 24, A. mytili W112-28; 25, ‘A. neptunis’ F146-38; 26, A. nitrofrigilis DSM 7299^T; 27, ‘A. ponticus’ F161-33; 28, ‘A. porcinus’ LMG 24487; 29, ‘A. salis’ F155-33; 30, A. skirrowii LMG 6621^T; 31, A. suis CECT 7833^T; 32, A. thereius LMG 24486^T; 33, A. trophiarum LMG 25534^T; 34, A. venerupis CECT 7836^T; 35, ‘A. viscosus’ F142-34; 36, ‘A. vitoriensis’ F199.