Characterization of a marine gammaproteobacterium capable of aerobic anoxygenic photosynthesis

Abstract

Members of the gammaproteobacterial clade NOR5/OM60 regularly form an abundant part, up to 11%, of the bacterioplankton community in coastal systems during the summer months. Here, we report the nearly complete genome sequence of one cultured representative, Congregibacter litoralis strain KT71, isolated from North Sea surface water. Unexpectedly, a complete photosynthesis superoperon, including genes for accessory pigments, was discov- from a surface water sample taken near the North Sea island Helgoland, by direct plating on complex low-nutrient media. Phylogenetic analysis showed that KT71 was the first cultured representative of a cosmopolitan gammaproteobacterial lineage, which we in the following refer to as the NOR5/OM60 clade (Fig. 1). The first indication for this clade dates back to 1997, when Rappe et al. retrieved two 16S rRNA clones, OM60 and OM241, from the continental shelf off Cape Hatteras, NC (2). In the following years, many sequences have been retrieved that were related to the clone OM60 (e.g.,. By the end of 2005, Ͼ180 partial and full length 16S rRNA sequences available within the public databases were related to KT71 and OM60.KT71 is a Gram-negative, pleomorphic, strictly aerobic, and motile bacterium. It is of an average size of 2 ϫ 0.5 m, has a generation time of 4.5 h, and often grows in flocs. Based on this conspicuous trait and the site of isolation, the name Congregibacter litoralis has been proposed. A full taxonomic description of strain KT71 is currently ongoing (B.M.F., S.S., and R.A., unpublished work). Several more strains belonging to the NOR5/ OM60 clade were isolated off the coast of Oregon, in sterilized seawater, using a high-throughput dilution-to-extinction technique (9, 10). Meanwhile, representatives of the NOR5/OM60 clade were also isolated from Arctic sea ice (11) and coastal sediments (12,13).FISH with rRNA-targeted oligonucleotide probes for NOR5/ OM60 confirmed this clade as an abundant component of the bacterioplankton community in the North Sea around the island Helgoland (1). By the end of July 1998, up to 8% of the total bacterioplankton community comprised members of the NOR5/ OM60 clade (1). A second peak of NOR5/OM60 cells was visible in mid-June (6%). However, NOR5/OM60 was not detected by FISH during the winter months, October to March, suggesting a marked seasonality. The fraction of DNA-synthesizing NOR5/ OM60 cells seems to be quite variable. Active DNA synthesis could be detected in August but not in May 2002, even though NOR5/OM60 was present in high numbers in both samples (6% and 11% of total bacterioplankton cell, respectively) (14).In 2004, KT71 was selected for whole-genome sequencing as part of the Gordon and Betty Moore Foundation (GBMF) Marine Microbiology Initiative. Here, we present data derived from the analysis of the genome of strain KT71 and from ecophysiological experiments addressing some of the predictions derived from genome annotation. Results and Discussion Structure and Phylogenetic Analysis of the Photosynthesis (PS)Operon. The...

Bacterial diversity and biogeography in deep-sea surface sediments of the South Atlantic Ocean

“…These belonged mainly to families of psychrophilic microorganisms including Enterobacteriaceae, Alteromonadaceae, Oceanospirillaceae and Legionellaceae (Figure 3a). Among Diversity and biogeography in deep-sea sediments R Schauer et al these phylotypes 11 OTUs (12 sequences) clustered with the NOR5/OM60 clade that includes 'Congregibacter litoralis' strain KT71, the first marine aerobic anoxygenic phototrophic Gammaproteobacteria in culture (Fuchs et al, 2007;Yan et al, 2009 (Figures 3a and b) and to Cret-1F, BD1-1, PWP and South Ionian groups (11 OUT, 27 sequences). These groups included only 16S rRNA gene sequences that originated from other deep-sea or permanent cold marine habitats Li et al, 1999;Ravenschlag et al, 1999;Urakawa et al, 1999;Bowman and McCuaig, 2003;Polymenakou et al, 2005;Xu et al, 2005;Zhao and Zeng, 2005).…”

Towards a better understanding of microbial carbon flux in the sea*

“…Genome analysis of Pelagibacter ubique in the SAR11 clade, one of the principal bacterial components in the sea, revealed the smallest genome known for a free-living microorganism, also containing the PR gene (Giovannoni et al 2005a,b). Very recent reports on genomic adaptations to life in the marine environment include the characterization of Alpha-and Gammaproteobacteria capable of aerobic anoxygenic photosynthesis (Fuchs et al 2007, Swingley et al 2007, the discovery of polymer degradation potential and life on particles among Flavobacteria (Bauer et al 2006), and comparisons of the mechanisms to derive organic and inorganic nutrients from phytoplankton among marine Roseobacter . At the same time, large-scale environmental genome shotgun sequencing has provided marine microbial ecologists with challenging amounts of genetic and genomic information to explore (Venter et al 2004, Rusch et al 2007).…”

Environmental proteomics of microbial plankton in a highly productive coastal upwelling system

“…Genomic and proteomic analysis of some OMG group isolates indicates these organisms contribute to carbon cycling using aerobic anoxygenic photosynthesis Fuchs et al, 2007). The majority of detected proteins from this group were best hits to OM60 clade isolates HTCC2080 and Congregibacter litoralis KT 71, which have been quantified, respectively, at 3.4% and up to 11% of the bacterial cells in coastal surface water Fuchs et al, 2007). Proteins from the SAR92 clade isolate HTCC 2207 (Stingl et al, 2007) and the BD1-7 clade isolate HTCC2143 (Cho and Giovannoni, 2004) were also detected.…”