Analysis of 1,000+ Type-Strain Genomes Substantially Improves Taxonomic Classification of Alphaproteobacteria - PubMed (original) (raw)

Analysis of 1,000+ Type-Strain Genomes Substantially Improves Taxonomic Classification of _Alphaproteobacteria

Anton Hördt et al. Front Microbiol. 2020.

Abstract

The class Alphaproteobacteria is comprised of a diverse assemblage of Gram-negative bacteria that includes organisms of varying morphologies, physiologies and habitat preferences many of which are of clinical and ecological importance. Alphaproteobacteria classification has proved to be difficult, not least when taxonomic decisions rested heavily on a limited number of phenotypic features and interpretation of poorly resolved 16S rRNA gene trees. Despite progress in recent years regarding the classification of bacteria assigned to the class, there remains a need to further clarify taxonomic relationships. Here, draft genome sequences of a collection of genomes of more than 1000 Alphaproteobacteria and outgroup type strains were used to infer phylogenetic trees from genome-scale data using the principles drawn from phylogenetic systematics. The majority of taxa were found to be monophyletic but several orders, families and genera, including taxa recognized as problematic long ago but also quite recent taxa, as well as a few species were shown to be in need of revision. According proposals are made for the recognition of new orders, families and genera, as well as the transfer of a variety of species to other genera and of a variety of genera to other families. In addition, emended descriptions are given for many species mainly involving information on DNA G+C content and (approximate) genome size, both of which are confirmed as valuable taxonomic markers. Similarly, analysis of the gene content was shown to provide valuable taxonomic insights in the class. Significant incongruities between 16S rRNA gene and whole genome trees were not found in the class. The incongruities that became obvious when comparing the results of the present study with existing classifications appeared to be caused mainly by insufficiently resolved 16S rRNA gene trees or incomplete taxon sampling. Another probable cause of misclassifications in the past is the partially low overall fit of phenotypic characters to the sequence-based tree. Even though a significant degree of phylogenetic conservation was detected in all characters investigated, the overall fit to the tree varied considerably.

Keywords: G+C content; Genome BLAST Distance Phylogeny; chemotaxonomy; genome size; morphology; phylogenetic systematics; phylogenomics.

Copyright © 2020 Hördt, López, Meier-Kolthoff, Schleuning, Weinhold, Tindall, Gronow, Kyrpides, Woyke and Göker.

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Figures

FIGURE 1

FIGURE 1

Overview of the phylogenomic tree inferred with FastME from GBDP distances calculated from whole proteomes. The numbers above branches are GBDP pseudo-bootstrap support values from 100 replications. Collapsed clades are displayed as triangles whose side lengths are proportional to the branch-length distances to least and most distant leave, respectively. The total number (#) of leaves per collapsed clade is shown within the triangles. The legend indicates the symbols and colors used in all subsequent figures, which show details of all clades of interest. In Figure 1 itself only the phylum is annotated, while Figures 2–9 show specific sections of the same tree in greater detail with the same underlying topology yet some differences in clade ordering. Clades not referred to in the text are not shown in detail in the subsequent figures but are displayed in Supplementary File S2. *phylogenetically including some taxa placed in Rhodobacterales, ** phylogenetically including some taxa placed in Rhizobiales.

FIGURE 2

FIGURE 2

First part of the GBDP tree shown in Figure 1, focussing on the phylum Spirochaetes as well as Rhodospirillales, Rickettsiales and Kiloniellales within the class Alphaproteobacteria. The clade labeled CEKPRRRS comprises the orders Caulobacterales, Emcibacterales, Kordiimonadales, Parvularculales, Rhizobiales (Hyphomicrobiales), Rhodobacterales, Rhodothalassiales, and Sneathiellales, details for which are shown in the subsequent figures. Tip labels with light-blue background indicate type species of genera, colors and symbols to the right of the tips indicate, from left to right, phylum, class, order, and family; for details and abbreviations see Figure 1. The blue color gradient indicates the G+C content as calculated from the genome sequences, followed by black bars indicating the (approximate) genome size in base pairs.

FIGURE 3

FIGURE 3

Second part of the GBDP tree shown in Figure 1, focussing on parts of Rhizobiales (Hyphomicrobiales). The clade labeled EKRS comprises the orders Emcibacterales, Kordiimonadales, Rhodothalassiales, and Sneathiellales, whereas CPR denotes the clade including the orders Caulobacterales, Parvularculales, and Rhodobacterales, details for which are shown in the subsequent figures. Tip labels with light-blue background indicate type species of genera, colors and symbols to the right of the tips indicate, from left to right, phylum, class, order and family; for details and abbreviations see Figure 1. The blue color gradient indicates the G+C content as calculated from the genome sequences, followed by black bars indicating the (approximate) genome size in base pairs.

FIGURE 4

FIGURE 4

Third part of the GBDP tree shown in Figure 1, focussing on parts of Rhizobiales (Hyphomicrobiales). The clade labeled EKRS comprises the orders Emcibacterales, Kordiimonadales, Rhodothalassiales and Sneathiellales, whereas CPR denotes the clade including the orders Caulobacterales, Parvularculales, and Rhodobacterales, details for which are shown in the subsequent figures. Tip labels with light-blue background indicate type species of genera, colors and symbols to the right of the tips indicate, from left to right, phylum, class, order and family; for details and abbreviations see Figure 1. The blue color gradient indicates the G+C content as calculated from the genome sequences, followed by black bars indicating the (approximate) genome size in base pairs.

FIGURE 5

FIGURE 5

Fourth part of the GBDP tree shown in Figure 1, focussing on parts of Rhizobiales (Hyphomicrobiales). The clade labeled EKRS comprises the orders Emcibacterales, Kordiimonadales, Rhodothalassiales and Sneathiellales, whereas CPR denotes the clade including the orders Caulobacterales, Parvularculales, and Rhodobacterales, details for which are shown in the subsequent figures. Tip labels with light-blue background indicate type species of genera, colors and symbols to the right of the tips indicate, from left to right, phylum, class, order, and family; for details and abbreviations see Figure 1. The blue color gradient indicates the G+C content as calculated from the genome sequences, followed by black bars indicating the (approximate) genome size in base pairs.

FIGURE 6

FIGURE 6

Fifth part of the GBDP tree shown in Figure 1, focussing on Sphingomonadales. The clade labeled CEKKPRRRRS comprises the orders Caulobacterales, Emcibacterales, Kiloniellales, Kordiimonadales, Parvularculales, Rhizobiales (Hyphomicrobiales), Rhodobacterales, Rhodospirillales, Rhodothalassiales, and Sneathiellales, details for which are shown in other figures. Tip labels with light-blue background indicate type species of genera, colors and symbols to the right of the tips indicate, from left to right, phylum, class, order, and family; for details and abbreviations see Figure 1. The blue color gradient indicates the G+C content as calculated from the genome sequences, followed by black bars indicating the (approximate) genome size in base pairs. Sphingomonas sanxanigenens DSM 19645 is represented by two genome sequences (SAMN02641489, above; SAMN02745820, below).

FIGURE 7

FIGURE 7

Sixth part of the GBDP tree shown in Figure 1, focussing on parts of Rhodobacterales. The clade labeled EKRS comprises the orders Emcibacterales, Kordiimonadales, Rhodothalassiales, and Sneathiellales, details for which are shown in other figures. Tip labels with light-blue background indicate type species of genera, colors and symbols to the right of the tips indicate, from left to right, phylum, class, order and family; for details and abbreviations see Figure 1. The blue color gradient indicates the G+C content as calculated from the genome sequences, followed by black bars indicating the (approximate) genome size in base pairs. Rhodobacter veldkampii DSM 11550 is represented by two genome sequences (SAMN10866319, above; SAMN08535030, below).

FIGURE 8

FIGURE 8

Seventh part of the GBDP tree shown in Figure 1, focussing on Caulobacterales, Parvularculales and parts of Rhodobacterales. Tip labels with light-blue background indicate type species of genera, colors and symbols to the right of the tips indicate, from left to right, phylum, class, order, and family; for details and abbreviations see Figure 1. The blue color gradient indicates the G+C content as calculated from the genome sequences, followed by black bars indicating the (approximate) genome size in base pairs.

FIGURE 9

FIGURE 9

Eighth part of the GBDP tree shown in Figure 1, focussing on parts of Rhodobacterales. The clade labeled EKRS comprises the orders Emcibacterales, Kordiimonadales, Rhodothalassiales, and Sneathiellales, details for which are shown in other figures. Tip labels with light-blue background indicate type species of genera, colors and symbols to the right of the tips indicate, from left to right, phylum, class, order, and family; for details and abbreviations see Figure 1. The blue color gradient indicates the G+C content as calculated from the genome sequences, followed by black bars indicating the (approximate) genome size in base pairs.

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