Ecological genomics of marine Roseobacters

Abstract

Bacterioplankton of the marine Roseobacter clade have genomes that reflect a dynamic environment and diverse interactions with marine plankton. Comparative genome sequence analysis of three cultured representatives suggests that cellular requirements for nitrogen are largely provided by regenerated ammonium and organic compounds (polyamines, allophanate, and urea), while typical sources of carbon include amino acids, glyoxylate, and aromatic metabolites. An unexpectedly large number of genes are predicted to encode proteins involved in the production, degradation, and efflux of toxins and metabolites. A mechanism likely involved in cell-to-cell DNA or protein transfer was also discovered: vir-related genes encoding a type IV secretion system typical of bacterial pathogens. These suggest a potential for interacting with neighboring cells and impacting the routing of organic matter into the microbial loop. Genes shared among the three roseobacters and also common in nine draft Roseobacter genomes include those for carbon monoxide oxidation, dimethylsulfoniopropionate demethylation, and aromatic compound degradation. Genes shared with other cultured marine bacteria include those for utilizing sodium gradients, transport and metabolism of sulfate, and osmoregulation.

FIG. 1.

Phylogenetic tree of 16S rRNA gene sequences from 12 roseobacters and other selected marine bacterioplankton for which a genome sequence is available. The tree is based on positions 21 to 1490 of the 16S rRNA gene (E. coli numbering system). The tree was constructed with the PAUP* package (53), version 4.10b, using the maximum likelihood method. The bar corresponds to the number of changes per nucleotide for the main tree.

FIG. 2.

Signal transduction proteins in three Roseobacter genomes and two comparison groups consisting of marine bacterioplankton or closely related nonmarine Alphaproteobacteria. The abundance of genes encoding signal transduction proteins are shown as percentages of total coding sequences (% of genome) or as numbers of the one-component systems AsnC/Lrp (likely involved in amino acid metabolism), GntR (repression of gluconate utilization), IclR (repression of the acetate operon), MarR (repression of antibiotic resistance or stress response), and TetR (repression of tetracycline resistance). The marine comparison group consists of 37 genomes with an average size of 4.0 Mb, while the nonmarine alphaproteobacterial comparison group consists of 8 genomes with an average size of 5.5 Mb.

FIG. 3.

Six distinct ring-cleaving pathways present in three Roseobacter genomes. Shaded tabs indicate the presence of a pathway (light gray, S. pomeroyi; dark gray, Silicibacter sp. strain TM1040; medium gray, Jannaschia sp. strain CCS1). The gene(s) encoding the ring-cleaving enzymes is chromosomally located unless otherwise indicated within the tab. *, S. pomeroyi contains two copies of the gentisate pathway: one on the chromosome and one on megaplasmid pSPD. The arrowheads leading into the TCA cycle indicate multiple steps. CoA, coenzyme A.

FIG. 4.

Genes for acquisition of nitrogen and phosphorus in three Roseobacter genomes. Shaded arrows indicate the presence of a pathway (light gray, S. pomeroyi; dark gray, Silicibacter sp. strain TM1040; medium gray, Jannaschia sp. strain CCS1). Numbers in colored circles indicate the number of ORFs if ≥2 copies. Amino acid transporters and branched-chain amino acid transporters are summed. C-O-P, phosphoesters; C-P, phosphonates; Pi, phosphate.

FIG. 5.

Roseobacter core genes (dark) and total genes (dark plus light) as a function of increasing genome number. Core genes are those with an RBH to the S. pomeroyi DSS-3 genome for the indicated genome plus all preceding genomes. Total genes are distinct genes in the Roseobacter group, incremented for each genome by the number of genes without an RBH in any of the preceding genomes.