Adaptation of an abundant Roseobacter RCA organism to pelagic systems revealed by genomic and transcriptomic analyses

Abstract

The RCA (Roseobacter clade affiliated) cluster, with an internal 16S rRNA gene sequence similarity of 498%, is the largest cluster of the marine Roseobacter clade and most abundant in temperate to (sub)polar oceans, constituting up to 35% of total bacterioplankton. The genome analysis of the first described species of the RCA cluster, Planktomarina temperata RCA23, revealed that this phylogenetic lineage is deeply branching within the Roseobacter clade. It shares not 465.7% of homologous genes with any other organism of this clade. The genome is the smallest of all closed genomes of the Roseobacter clade, exhibits various features of genome streamlining and encompasses genes for aerobic anoxygenic photosynthesis (AAP) and CO oxidation. In order to assess the biogeochemical significance of the RCA cluster we investigated a phytoplankton spring bloom in the North Sea. This cluster constituted 5.1% of the total, but 10-31% (mean 18.5%) of the active bacterioplankton. A metatranscriptomic analysis showed that the genome of P. temperata RCA23 was transcribed to 94% in the bloom with some variations during day and night. The genome of P. temperata RCA23 was also retrieved to 84% from metagenomic data sets from a Norwegian fjord and to 82% from stations of the Global Ocean Sampling expedition in the northwestern Atlantic. In this region, up to 6.5% of the total reads mapped on the genome of P. temperata RCA23. This abundant taxon appears to be a major player in ocean biogeochemistry.

Ecological Genomics of the Uncultivated Marine Roseobacter Lineage CHAB-I-5

“…The other two, largely uncultivated lineages, NAC11-7 and DC5-80-3, are part of the basal lineages of the Roseobacter clade ( Fig. 1), which is again consistent with other studies (5,17). Genome streamlining of marine planktonic bacteria may be an important cause of their resistance to cultivation (10,11).…”

“…They consistently have streamlined (2.6 to 3.5 Mbp) and GϩC-poor (39 to 40%) genomes, a reduced percentage of noncoding DNA, and a gene repertoire matching that of the free-living model (14). These features are also evident in another two Roseobacter lineages, NAC11-7 (15)(16)(17) and DC5-80-3 (or RCA, or Planktomarina temperata in ARB SILVA) (17). They are among the most abundant bacteria in some ocean regions such as Monterey Bay (18) and the North Sea (4), respectively, but remain largely uncultivated.…”

“…the latter are based on a single PR gene, the former require a photosynthesis gene cluster (PGC) that is composed of genes coding for a photosynthetic reaction center, light harvesting complexes, BChl, carotenoids, and assembly factors (59). Previous studies showed that the representative strain HTCC2255 of lineage NAC11-7 is the only known Roseobacter that uses PR to harvest light energy (5) and that the type strain Planktomarina temperata RCA23 of lineage DC5-80-3 is an AAP (17). We identified a complete and partial PGC in the SAG-O19 lineage (found in AAA298-K06) and in the CHAB-I-5 lineage, respectively (see Fig.…”

“…A previous study partitioned the cultured roseobacters into two lifestyle groups, those from pelagic oceans and those from associations with other organisms, surfaces, or sediments (17). To understand the ecological success of the four largely uncultivated lineages, we selected six cultured and phylogenetically diverse (Fig.…”

Global occurrence and heterogeneity of the Roseobacter-clade species Ruegeria mobilis

“…The R. mobilis strains described herein can potentially be classified as copiotroph representatives of the Roseobacter clade due to their genome size and genomic features (Luo and Moran, 2014;Voget et al, 2014). As they were isolated from a wide variety of ecological niches, they might contribute substantially to the total Roseobacter gene repertoire (Moran et al, 2007).…”