Silicibacter pomeroyi sp. nov. and Roseovarius nubinhibens sp. nov., dimethylsulfoniopropionate-demethylating bacteria from marine environments

González, José M.; Covert, Joseph S.; Whitman, William B.; Henriksen, James R.; Mayer, Frank; Scharf, Birgit E.; Schmitt, Rüdiger; Buchan, Alison; Fuhrman, Jed A.; Kiene, Ronald P.; Moran, Mary Ann

doi:10.1099/ijs.0.02491-0

Cited by 223 publications

(140 citation statements)

References 36 publications

Supporting

Mentioning

135

Contrasting

Order By: Relevance

“…Silicibacter pomeroyi DSS-3 was derived from a marine dimethylsulfoniopropionate enrichment culture (16,17). Finally, two isolates that were not obtained from the southeastern U.S. coast were examined: Sulfitobacter pontiacus ChLG 10, which was cultured from the Black Sea (43), and Roseovarius nubinhibens ISM, which was cultured from the Caribbean Sea (14,16).…”

Section: Methodsmentioning

confidence: 99%

Diverse Organization of Genes of the β-Ketoadipate Pathway in Members of the Marine Roseobacter Lineage

Buchan¹,

Neidle

Moran³

2004

Appl Environ Microbiol

Self Cite

View full text Add to dashboard Cite

Members of the Roseobacter lineage, an ecologically important marine clade within the class ␣-Proteobacteria, harbor genes for the protocatechuate branch of the ␤-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 ␤-ketoadipate pathway.

show abstract

Section: Methodsmentioning

confidence: 99%

Diverse Organization of Genes of the β-Ketoadipate Pathway in Members of the Marine Roseobacter Lineage

Buchan¹,

Neidle

Moran³

2004

Appl Environ Microbiol

Self Cite

View full text Add to dashboard Cite

show abstract

“…Ecologically relevant representatives of the MRC are readily cultivated and amenable to genetic manipulation, thereby making them good model organisms to investigate bacterial ecophysiology in the marine environment. Ruegeria pomeroyi DSS-3, isolated off the coast of Oregon in the United States (35), is the best characterized model marine organism in this clade (32,(36)(37)(38)(39).…”

Section: Significancementioning

confidence: 99%

Trimethylamine N -oxide metabolism by abundant marine heterotrophic bacteria

Lidbury

Murrell

Chen

2014

Proc. Natl. Acad. Sci. U.S.A.

128

191

View full text Add to dashboard Cite

Trimethylamine N-oxide (TMAO) is a common osmolyte found in a variety of marine biota and has been detected at nanomolar concentrations in oceanic surface waters. TMAO can serve as an important nutrient for ecologically important marine heterotrophic bacteria, particularly the SAR11 clade and marine Roseobacter clade (MRC). However, the enzymes responsible for TMAO catabolism and the membrane transporter required for TMAO uptake into microbial cells have yet to be identified. We show here that the enzyme TMAO demethylase (Tdm) catalyzes the first step in TMAO degradation. This enzyme represents a large group of proteins with an uncharacterized domain (DUF1989). The function of TMAO demethylase in a representative from the SAR11 clade (strain HIMB59) and in a representative of the MRC (Ruegeria pomeroyi DSS-3) was confirmed by heterologous expression of tdm (the gene encoding Tdm) in Escherichia coli. In R. pomeroyi, mutagenesis experiments confirmed that tdm is essential for growth on TMAO. We also identified a unique ATP-binding cassette transporter (TmoXWV) found in a variety of marine bacteria and experimentally confirmed its specificity for TMAO through marker exchange mutagenesis and lacZ reporter assays of the promoter for genes encoding this transporter. Both Tdm and TmoXWV are particularly abundant in natural seawater assemblages and actively expressed, as indicated by a number of recent metatranscriptomic and metaproteomic studies. These data suggest that TMAO represents a significant, yet overlooked, nutrient for marine bacteria. (1) and is predicted to have a number of important physiological roles (2). In marine elasmobranchs (sharks and rays), TMAO accumulates at high concentrations (up to 500 mM), helping to offset the destabilizing effects of urea on cellular proteins (1, 3, 4). TMAO can be metabolized to small methylated amines, for example, tri-, di-, and monomethylamine (TMA, DMA, and MMA, respectively). These volatile organic N compounds are precursors of marine aerosols and the potent greenhouse gas nitrous oxide in the marine atmosphere (5). In anoxic sediments or pockets of hypoxic conditions, such as in marine snow, they are precursors for the potent greenhouse gas methane (6). In marine surface waters, TMAO concentrations can reach up to 79 nM; however, owing to the technical difficulties associated with quantifying TMAO in seawater, reports of in situ concentrations of TMAO are limited (7,8). In a previously published study in which TMAO and TMA were quantified in the marine environment, TMAO had a higher average concentration throughout the water column and over a seasonal cycle (8).TMAO is a well-studied terminal electron acceptor for anaerobic microbial respiration (9, 10), but its catabolism in aerobic surface seawater is not well understood. Recent studies have shown that TMAO in the Sargasso Sea is predominantly oxidized by bacterioplankton as an energy source (11) and that the marine methylotrophic bacterium Methylophilales sp. HTCC2181 oxidizes TMAO to CO 2 to generate energy (1...

show abstract

“…Agar plates were prepared with purified agar at 0.8% w/v and kept aerobically in a temperature-controlled incubator (20 1C). Alternatively, several Roseobacter and Rhodobacter strains were obtained from Chesapeake Bay in April 2008 and Virginia Beach in March 2007 by using the previously described DMSP enrichment method (González et al, 2003) with some modification. Sea water samples were diluted with sterilized artificial sea water, then amended with 100 mM DMSP.…”

Section: Isolation Of Roseobacter and Rhodobactermentioning

confidence: 99%

Gene transfer agent (GTA) genes reveal diverse and dynamic Roseobacter and Rhodobacter populations in the Chesapeake Bay

et al. 2008

Self Cite

View full text Add to dashboard Cite

Within the bacterial class Alphaproteobacteria, the order Rhodobacterales contains the Roseobacter and Rhodobacter clades. Roseobacters are abundant and play important biogeochemical roles in marine environments. Roseobacter and Rhodobacter genomes contain a conserved gene transfer agent (GTA) gene cluster, and GTA-mediated gene transfer has been observed in these groups of bacteria. In this study, we investigated the genetic diversity of these two groups in Chesapeake Bay surface waters using a specific PCR primer set targeting the conserved Rhodobacterales GTA major capsid protein gene (g5). The g5 gene was successfully amplified from 26 Rhodobacterales isolates and the bay microbial communities using this primer set. Four g5 clone libraries were constructed from microbial assemblages representing different regions and seasons of the bay and yielded diverse sequences. In total, 12 distinct g5 clusters could be identified among 158 Chesapeake Bay clones, 11 fall within the Roseobacter clade, and one falls in the Rhodobacter clade. The vast majority of the clusters (10 out of 12) lack cultivated representatives. The composition of g5 sequences varied dramatically along the bay during the wintertime, and a distinct Roseobacter population composition between winter and summer was observed. The congruence between g5 and 16S rRNA gene phylogenies indicates that g5 may serve as a useful genetic marker to investigate diversity and abundance of Roseobacter and Rhodobacter in natural environments. The presence of the g5 gene in the natural populations of Roseobacter and Rhodobacter implies that genetic exchange through GTA transduction could be an important mechanism for maintaining the metabolic flexibility of these groups of bacteria.

show abstract

Silicibacter pomeroyi sp. nov. and Roseovarius nubinhibens sp. nov., dimethylsulfoniopropionate-demethylating bacteria from marine environments

Cited by 223 publications

References 36 publications

Diverse Organization of Genes of the β-Ketoadipate Pathway in Members of the Marine Roseobacter Lineage

Diverse Organization of Genes of the β-Ketoadipate Pathway in Members of the Marine Roseobacter Lineage

Trimethylamine N -oxide metabolism by abundant marine heterotrophic bacteria

Gene transfer agent (GTA) genes reveal diverse and dynamic Roseobacter and Rhodobacter populations in the Chesapeake Bay

Contact Info

Product

Resources

About