Dataset Information

Diverse organization of genes of the beta-ketoadipate pathway in members of the marine Roseobacter lineage.

ABSTRACT: Members of the Roseobacter lineage, an ecologically important marine clade within the class alpha-Proteobacteria, harbor genes for the protocatechuate branch of the beta-ketoadipate pathway, a major catabolic route for lignin-related aromatic compounds. The genes of this pathway are typically clustered, although gene order varies among organisms. Here we characterize genes linked to pcaH and -G, which encode protocatechuate 3,4-dioxygenase, in eight closely related members of the Roseobacter lineage (pairwise 16S rRNA gene sequence identities, 92 to 99%). Sequence analysis of genomic fragments revealed five unique pca gene arrangements. Identical gene organization was found for isolates demonstrating species-level identity (i.e., >99% 16S rRNA gene similarity). In one isolate, six functionally related genes were clustered: pcaQ, pobA, pcaD, pcaC, pcaH, and pcaG. The remaining seven isolates lacked at least one of these genes in their clusters, although the relative order of the remaining genes was preserved. Three genes (pcaC, -H, and -G) were physically linked in all isolates. A highly conserved open reading frame (ORF) was found immediately downstream of pcaG in all eight isolates. Reverse transcription-PCR analysis of RNA from one isolate, Silicibacter pomeroyi DSS-3, provides evidence that this ORF is coexpressed with upstream pca genes. The absence of this ORF in similar bacterial pca gene clusters from diverse microbes suggests a niche-specific role for its protein product in Roseobacter group members. Collectively, these comparisons of bacterial pca gene organization illuminate a complex evolutionary history and underscore the widespread ecological importance of the encoded beta-ketoadipate pathway.

SUBMITTER: Buchan A

PROVIDER: S-EPMC368412 | biostudies-literature | 2004 Mar

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Diverse organization of genes of the beta-ketoadipate pathway in members of the marine Roseobacter lineage.

Buchan Alison A Neidle Ellen L EL Moran Mary Ann MA

Applied and environmental microbiology 20040301 3

Members of the Roseobacter lineage, an ecologically important marine clade within the class alpha-Proteobacteria, harbor genes for the protocatechuate branch of the beta-ketoadipate pathway, a major catabolic route for lignin-related aromatic compounds. The genes of this pathway are typically clustered, although gene order varies among organisms. Here we characterize genes linked to pcaH and -G, which encode protocatechuate 3,4-dioxygenase, in eight closely related members of the Roseobacter lin ...[more]

PMID: 15006791

Similar Datasets

Project description:Many major marine bacterial lineages such as SAR11, Prochlorococcus, SAR116, and several Roseobacter lineages have members that are abundant, relatively slow-growing, and genome streamlined. The isolation of phages that infect SAR11 and SAR116 have demonstrated the dominance of these phages in the marine virosphere. However, no phages have been isolated from bacteria in the Roseobacter RCA lineage, another abundant group of marine bacteria. In this study, seven RCA phages that infect three different RCA strains were isolated and characterized. All seven RCA phages belong to the Podoviridae family and have genome sizes ranging from 39.6 to 58.1 kb. Interestingly, three RCA phages (CRP-1, CRP-2, and CRP-3) show similar genomic content and architecture as SAR116 phage HMO-2011, which represents one of the most abundant known viral groups in the ocean. The high degree of homology among CRP-1, CRP-2, CRP-3, and HMO-2011 resulted in the contribution of RCA phages to the dominance of the HMO-2011-type group. CRP-4 and CRP-5 are similar to the Cobavirus group roseophages in terms of gene content and organization. The remaining two RCA phages, CRP-6 and CRP-7, show limited genomic similarity with known phages and represent two new phage groups. Metagenomic fragment recruitment analyses reveal that these RCA phage groups are much more abundant in the ocean than most existing marine roseophage groups. The characterization of these RCA phages has greatly expanded our understanding of the genomic diversity and evolution of marine roseophages and suggests the critical need for isolating phages from the abundant but "unculturable" bacteria.IMPORTANCE The RCA lineage of the marine Roseobacter group represents one of the slow-growing but dominant components of marine microbial communities. Although dozens of roseophages have been characterized, no phages infecting RCA strains have been reported. In this study, we reported on the first RCA phage genomes and investigated their distribution pattern and relative abundance in comparison with other important marine phage groups. Two of the four RCA phage groups were found closely related to previously reported SAR116 phage HMO-2011 and Cobavirus group roseophages, respectively. The remaining two groups are novel in the genome contents. Our study also revealed that RCA phages are widely distributed and exhibit high abundance in marine viromic data sets. Altogether, our findings have greatly broadened our understanding of RCA phages and emphasize the ecological and evolutionary importance of RCA phages in the marine virosphere.

Project description:BackgroundIn the present work the central carbon metabolism of Dinoroseobacter shibae and Phaeobacter gallaeciensis was studied at the level of metabolic fluxes. These two strains belong to the marine Roseobacter clade, a dominant bacterial group in various marine habitats, and represent surface-associated, biofilm-forming growth (P. gallaeciensis) and symbiotic growth with eukaryotic algae (D. shibae). Based on information from recently sequenced genomes, a rich repertoire of pathways has been identified in the carbon core metabolism of these organisms, but little is known about the actual contribution of the various reactions in vivo.ResultsUsing 13C labelling techniques in specifically designed experiments, it could be shown that glucose-grown cells of D. shibae catabolise the carbon source exclusively via the Entner-Doudoroff pathway, whereas alternative routes of glycolysis and the pentose phosphate pathway are obviously utilised for anabolic purposes only. Enzyme assays confirmed this flux pattern and link the lack of glycolytic flux to the absence of phosphofructokinase activity. The previously suggested formation of phosphoenolpyruvate from pyruvate during mixotrophic CO2 assimilation was found to be inactive under the conditions studied. Moreover, it could be shown that pyruvate carboxylase is involved in CO2 assimilation and that the cyclic respiratory mode of the TCA cycle is utilised. Interestingly, the use of intracellular pathways was highly similar for P. gallaeciensis.ConclusionThe present study reveals the first insight into pathway utilisation within the Roseobacter group. Fluxes through major intracellular pathways of the central carbon metabolism, which are closely linked to the various important traits found for the Roseobacter clade, could be determined. The close similarity of fluxes between the two physiologically rather different species might provide the first indication of more general key properties among members of the Roseobacter clade which may explain their enormous success in the marine realm.

Dataset Information

Diverse organization of genes of the beta-ketoadipate pathway in members of the marine Roseobacter lineage.

Publications

Diverse organization of genes of the beta-ketoadipate pathway in members of the marine Roseobacter lineage.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets