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. 2017 Jun;11(6):1483-1499.
doi: 10.1038/ismej.2016.198. Epub 2017 Jan 20.

Phylogenomics of Rhodobacteraceae Reveals Evolutionary Adaptation to Marine and Non-Marine Habitats

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Free PMC article

Phylogenomics of Rhodobacteraceae Reveals Evolutionary Adaptation to Marine and Non-Marine Habitats

Meinhard Simon et al. ISME J. .
Free PMC article

Abstract

Marine Rhodobacteraceae (Alphaproteobacteria) are key players of biogeochemical cycling, comprise up to 30% of bacterial communities in pelagic environments and are often mutualists of eukaryotes. As 'Roseobacter clade', these 'roseobacters' are assumed to be monophyletic, but non-marine Rhodobacteraceae have not yet been included in phylogenomic analyses. Therefore, we analysed 106 genome sequences, particularly emphasizing gene sampling and its effect on phylogenetic stability, and investigated relationships between marine versus non-marine habitat, evolutionary origin and genomic adaptations. Our analyses, providing no unequivocal evidence for the monophyly of roseobacters, indicate several shifts between marine and non-marine habitats that occurred independently and were accompanied by characteristic changes in genomic content of orthologs, enzymes and metabolic pathways. Non-marine Rhodobacteraceae gained high-affinity transporters to cope with much lower sulphate concentrations and lost genes related to the reduced sodium chloride and organohalogen concentrations in their habitats. Marine Rhodobacteraceae gained genes required for fucoidan desulphonation and synthesis of the plant hormone indole 3-acetic acid and the compatible solutes ectoin and carnitin. However, neither plasmid composition, even though typical for the family, nor the degree of oligotrophy shows a systematic difference between marine and non-marine Rhodobacteraceae. We suggest the operational term 'Roseobacter group' for the marine Rhodobacteraceae strains.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
ML tree inferred from the core-gene matrix (208 genes, 80 578 characters) under a single overall model of amino-acid evolution and rooted with the included outgroup strains. The branches are scaled in terms of the expected number of substitutions per site; double slashes indicate branches shortened by 90%. Numbers above branches (from left to right) are bootstrapping support values if >60% from (i) ordinary bootstrap under ML with a single overall model of amino-acid evolution; (ii) ordinary bootstrap under ML with one model per gene; (iii) partition bootstrap under ML; (iv) ordinary bootstrap under MP; and (v) partition bootstrap under MP. Values >95% are shown in bold; dots indicate branches with maximum support under all settings. The inferred major clades are indicated with numbers and colours; clade 2 comprises all ingroup strains not assigned to the Roseobacter group. Triangles indicate type strains. The colours of the tip labels indicate the habitat: blue, marine; brown, non-marine; uncoloured, unknown.
Figure 2
Figure 2
Ancestral character-state reconstruction under ordered MP for the presence (black) or absence (white) of H, marine or equivalent habitat; I, (S)-2-haloacid dehalogenase (EC 3.8.1.2); II, ectoine synthase (EC 4.2.1.108); and III, 6-phosphofructokinase (EC 2.7.1.11). The tree topology and the number and colour codes for the major clades are as in Figure 1. Grey shading indicates uncertainties in character-state assignment. The major types of phylogenetic distributions represented by the three genomic characters are: I, losses predominantly in non-marine strains; II, gains mainly in marine strains; and III, gains predominantly in non-marine strains.
Figure 3
Figure 3
Ancestral character-state reconstruction under ordered MP for the number of ECR replicases of the distinct types DnaA, RepA, RepB and RepABC and according pairwise phylogenetic cross-comparisons of their abundances in each genome. For the labels of the tips, see Figure 2, where the same tree topology is depicted in exactly the same layout. The number and colour codes between the trees refer to the clades as indicated in Figure 1 (O=outgroup). The colours depicted on the topologies indicate the number of replicases of each type as follows: white, 0; blue, 1; green, 2; yellow, 3; orange, 4; red, 5; and black, 6. Presences and absences alone are correlated between DnaA, RepA and RepB but not between RepABC and the others.
Figure 4
Figure 4
A summary of the interpretation of the genetic traits of the most recent marine ancestor of Rhodobacteraceae significantly gained or lost during adaptation to non-marine and gained during better adaptation to marine habitats.

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