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Transformation of sulfur compounds by an abundant lineage of marine bacteria in the alpha-subclass of the class Proteobacteria.

ABSTRACT: Members of a group of marine bacteria that is numerically important in coastal seawater and sediments were characterized with respect to their ability to transform organic and inorganic sulfur compounds. Fifteen strains representing the Roseobacter group (a phylogenetic cluster of marine bacteria in the alpha-subclass of the class Proteobacteria) were isolated from seawater, primarily from the southeastern United States. Although more than one-half of the isolates were obtained without any selection for sulfur metabolism, all of the isolates were able to degrade the sulfur-containing osmolyte dimethyl sulfoniopropionate (DMSP) with production of dimethyl sulfide (DMS). Five isolates also degraded DMSP with production of methanethiol, indicating that both cleavage and demethylation pathways for DMSP occurred in the same organism, which is unusual. Five isolates were able to reduce dimethyl sulfoxide to DMS, and several isolates also degraded DMS and methanethiol. Sulfite oxygenase activity and methanesulfonic acid oxygenase activity were also present in some of the isolates. The ability to incorporate the reduced sulfur in DMSP and methanethiol into cellular material was studied with one of the isolates. A group-specific 16S rRNA probe indicated that the relative abundance of uncultured bacteria in the Roseobacter group increased in seawater enriched with DMSP or DMS. Because this group typically accounts for >10% of the 16S ribosomal DNA pool in coastal seawater and sediments of the southern United States, clues about its potential biogeochemical role are of particular interest. Studies of culturable representatives suggested that the group could mediate a number of steps in the cycling of both organic and inorganic forms of sulfur in marine environments.

SUBMITTER: Gonzalez JM

PROVIDER: S-EPMC99705 | biostudies-literature | 1999 Sep

REPOSITORIES: biostudies-literature

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Transformation of sulfur compounds by an abundant lineage of marine bacteria in the alpha-subclass of the class Proteobacteria.

González J M JM Kiene R P RP Moran M A MA

Applied and environmental microbiology 19990901 9

Members of a group of marine bacteria that is numerically important in coastal seawater and sediments were characterized with respect to their ability to transform organic and inorganic sulfur compounds. Fifteen strains representing the Roseobacter group (a phylogenetic cluster of marine bacteria in the alpha-subclass of the class Proteobacteria) were isolated from seawater, primarily from the southeastern United States. Although more than one-half of the isolates were obtained without any selec ...[more]

PMID: 10473380

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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:BACKGROUND:For decades it has been recognized that neutrophilic Fe-oxidizing bacteria (FeOB) are associated with hydrothermal venting of Fe(II)-rich fluids associated with seamounts in the world's oceans. The evidence was based almost entirely on the mineralogical remains of the microbes, which themselves had neither been brought into culture or been assigned to a specific phylogenetic clade. We have used both cultivation and cultivation-independent techniques to study Fe-rich microbial mats associated with hydrothermal venting at Loihi Seamount, a submarine volcano. METHODOLOGY/PRINCIPLE FINDINGS:Using gradient enrichment techniques, two iron-oxidizing bacteria, strains PV-1 and JV-1, were isolated. Chemolithotrophic growth was observed under microaerobic conditions; Fe(II) and Fe(0) were the only energy sources that supported growth. Both strains produced filamentous stalk-like structures composed of multiple nanometer sized fibrils of Fe-oxyhydroxide. These were consistent with mineralogical structures found in the iron mats. Phylogenetic analysis of the small subunit (SSU) rRNA gene demonstrated that strains PV-1 and JV-1 were identical and formed a monophyletic group deeply rooted within the Proteobacteria. The most similar sequence (85.3% similarity) from a cultivated isolate came from Methylophaga marina. Phylogenetic analysis of the RecA and GyrB protein sequences confirmed that these strains are distantly related to other members of the Proteobacteria. A cultivation-independent analysis of the SSU rRNA gene by terminal-restriction fragment (T-RF) profiling showed that this phylotype was most common in a variety of microbial mats collected at different times and locations at Loihi. CONCLUSIONS:On the basis of phylogenetic and physiological data, it is proposed that isolate PV-1(T) ( = ATCC BAA-1019: JCM 14766) represents the type strain of a novel species in a new genus, Mariprofundus ferrooxydans gen. nov., sp. nov. Furthermore, the strain is the first cultured representative of a new candidatus class of the Proteobacteria that is widely distributed in deep-sea environments, Candidatus zeta (zeta)-Proteobacteria cl. nov.

Dataset Information

Transformation of sulfur compounds by an abundant lineage of marine bacteria in the alpha-subclass of the class Proteobacteria.

Publications

Transformation of sulfur compounds by an abundant lineage of marine bacteria in the alpha-subclass of the class Proteobacteria.

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