Genome characteristics of a generalist marine bacterial lineage

Abstract

Members of the marine Roseobacter lineage have been characterized as ecological generalists, suggesting that there will be challenges in assigning well-delineated ecological roles and biogeochemical functions to the taxon. To address this issue, genome sequences of 32 Roseobacter isolates were analyzed for patterns in genome characteristics, gene inventory, and individual gene/ pathway distribution using three predictive frameworks: phylogenetic relatedness, lifestyle strategy and environmental origin of the isolate. For the first framework, a phylogeny containing five deeply branching clades was obtained from a concatenation of 70 conserved single-copy genes. Somewhat surprisingly, phylogenetic tree topology was not the best model for organizing genome characteristics or distribution patterns of individual genes/pathways, although it provided some predictive power. The lifestyle framework, established by grouping isolates according to evidence for heterotrophy, photoheterotrophy or autotrophy, explained more of the gene repertoire in this lineage. The environment framework had a weak predictive power for the overall genome content of each strain, but explained the distribution of several individual genes/pathways, including those related to phosphorus acquisition, chemotaxis and aromatic compound degradation. Unassembled sequences in the Global Ocean Sampling metagenomic data independently verified this global-scale geographical signal in some Roseobacter genes. The primary findings emerging from this comparative genome analysis are that members of the lineage cannot be easily collapsed into just a few ecologically differentiated clusters (that is, there are almost as many clusters as isolates); the strongest framework for predicting genome content is trophic strategy, but no single framework gives robust predictions; and previously unknown homologs to genes for H 2 oxidation, proteorhodopsin-based phototrophy, xanthorhodpsin-based phototrophy, and CO 2 fixation by Form IC ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) expand the possible mechanisms for energy and carbon acquisition in this remarkably versatile bacterial lineage.

Single-taxon field measurements of bacterial gene regulation controlling DMSP fate

“…In contrast, DMSPdegrading members of the Roseobacter and SAR116 lineages can, like HTCC2255, carry genes for both demethylation and cleavage (Newton et al, 2010;Moran et al, 2012), and therefore more directly influence the fate of DMSP. Emerging technological capabilities for conducting taxon-specific observations of gene regulation in the ocean are allowing us to explore, for the first time, the diversity of gene regulation strategies among the key bacterial groups affecting partitioning of organic sulfur between the ocean and atmosphere.…”

“…In the coastal upwelling system of Monterey Bay, CA, previous metagenomic and metatranscriptomic surveys indicated consistent and abundant populations of a bacterial taxon with high genetic relatedness to Roseobacter strain HTCC2255 (Ottesen et al, 2011), a bacterium capable of both DMSP cleavage and demethylation (Newton et al, 2010). We took advantage of the predictable presence of this bacterium to design HTC2255-specific PCR primers for in situ observations for the first committed step in each of the two DMSP degradation pathways.…”

The microbiome of North Sea copepods

“…Most of these phylotypes belong to the Roseobacter lineage. As ecological generalists, Roseobacter harbour large gene inventories and a remarkable suite of mechanisms by which to obtain carbon and energy (Newton et al 2010). Members of the Roseobacter lineage play an important role for the global carbon and sulphur cycle, for example, and are able to produce dimethylsulfide (DMS) (Wagner-Döbler and Biebl 2006).…”

Microdiversity of extracellular enzyme genes among sequenced prokaryotic genomes

“…For example, genomic analysis has allowed unprecedented insight into the environmental resource adaptation and ecological function of several key lineages, including Prochlorococcus (Rocap et al, 2003;Martiny et al, 2006), Synechococcus (Palenik et al, 2006), Roseobacter (Newton et al, 2010) and Escherichia coli (Luo et al, 2011). Since genome sequences represent the complete genetic repertoire of potential functions available to an organism, including strategies available for resource acquisition, the increasing availability of sequenced prokaryotic genomes holds much promise for clarifying taxon-trait relationships (Fraser et al, 2000;Ward and Klota, 2011).…”