Evolutionary ecology of the marine Roseobacter clade

Abstract

Members of the Roseobacter clade are equipped with a tremendous diversity of metabolic capabilities, which in part explains their success in so many different marine habitats. Ideas on how this diversity evolved and is maintained are reviewed, focusing on recent evolutionary studies exploring the timing and mechanisms of Roseobacter ecological diversification.

FIG 1

Survey of select genes and metabolic pathways in 52 Roseobacter isolate genomes. % complete, estimate of genome completeness; GTA, gene transfer agent; AAP, aerobic anoxygenic photoheterotrophy; PR, proteorhodopsin; XR, xanthorhodopsin; nasA, assimilatory nitrate reductase; nirB, assimilatory nitrite reductase; napA, periplasmic dissimilatory nitrate reductase; narG, dissimilatory nitrate reductase; nirS, dissimilatory nitrite reductase; nirK, dissimilatory nitrite reductase; dmdA, dimethylsulfoniopropionate demethylase; soxB, sulfur oxidation gene; coxL type I, carbon monoxide oxidation; B7, biotin synthase; B1, thiamine synthase; B12, cobalamin synthase; Type IV Sec, type IV secretion system. Colors indicate four major clades of isolate genomes. The phylogenetic tree was constructed based on a concatenation of ∼50 single-copy conserved protein sequences using the RAxML software.

FIG 2

Evolutionary time line of the Roseobacter lineage. (Left) The first predicted episode of Roseobacter genome expansion coincided with the radiation of marine dinoflagellates and coccolithophorids ∼250 mya. The diversification of diatoms occurred more recently. (Middle) Free-living and particle-associated roseobacters cooccur in the surface ocean, each with a distinct set of traits. (Right) In a future ocean, greater dominance by phytoplankton lineages with smaller cell sizes could lead to a decrease in particle-associated roseobacter populations.

FIG 3

Comparison of characteristics of cultured Roseobacter genomes, single-cell Roseobacter genomes, and Roseobacter sequences in the GOS metagenome. (Left) Distribution of G+C content. The arrow represents the mean value for the SAG genomes. (Right) Estimated average genome size plotted against the fraction of noncoding DNA.

FIG 4

Roseobacter sequences in metagenomic data sets, calculated as a percentage of free-living (0.1 to 0.8 μm) (green bars) and particle-associated (0.8 to 3.0 μm) (blue bars) reads in DNA from the Southern Ocean (13 stations [Stn.]) and Monterey Bay, CA (4 stations). Asterisks indicate significant differences between size fractions (P < 0.05). Data were obtained by analyzing 2,235 orthologous gene families shared by at least 20 of the 40 Roseobacter isolate genomes.