Silicibacter pomeroyi

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A Microbial Biorealm page on the genus Silicibacter pomeroyi

Classification

Higher order taxa

cellular organisms; Bacteria; Proteobacteria; Alphaproteobacteria; Rhodobacterales; Rhodobacteraceae; Silicibacter(12)

Evidence suggests that Silicibacter pomeroyi belongs to the Roseobacter lineage(5).

Species

NCBI: Taxonomy

Silicibacter pomeroyi

Description and significance

Silicibacter pomeroyi is among organisms that are capable of degrading sulfur compounds found in marine environments. In fact, this bacterium has the ability not only to degrade but also to demethylate and cleave dimethylsulfoniopropionate (DMSP). Silicibacter pomeroyi is a rod-shaped, Gram-negative bacterium that lives in marine environments and uses oxygen for its metabolic activities, such as to obtain energy. Silicibacter pomeroyi has a single but complex flagellum that rotates in the clockwise direction (5), which accounts for its motility (11). This important characteristic enables the organism to place itself in favorable environments(9). Its surface is covered with blebs, which are blister-like fluid-filled elevations of the skin, and its interior contains poly-β-hydroxybutyrate (PHB) inclusions. It was isolated in the state of Georgia, USA from coastal sea water (7). This organism should be given a lot of attention because it plays an important role in climate regulation and greatly contributes to the “global atmospheric sulfur pool” (5). By degrading DMSP, Silicibacter pomeroyi causes the formation of dimethylsulfide (DMS), which is a volatile sulfur compound that greatly adds to the sulfur supply in the atmosphere. DMS also influences climate regulation by forming clouds and backscattering solar radiation (3, 12).

In addition, this organism is also known to carry out the DMSP- demethylation/demethiolation pathway to produce methanethiol (MeSH) (9) (Figure 1). The significance of MeSH lies in its critical role in the incorporation of DMSP sulfur into bacterial proteins. In the presence of MeSH, sulfur obtained from the degradation of DMSP is quickly integrated into the bacterial proteins (9).

Genome structure

The genomic sequence of Silicibacter pomeroyi is 4,109,442 base pairs long. It contains a megaplasmid that is 491,611 base pairs long (11). The megaplasmid has no rRNA operons (10). The genome sequence also has 4,283 coding sequences (CDS). S. pomeroyi has a linear chromosome while DSS-3 has a circular chromosome. S. pomeroyi and DSS-3 are different strains of the same species (11). The existence of any prophages in the bacterial genome has not been detected. A unique and noteworthy characteristic of S. pomeroyi is that it has “the highest proportion of genes coding for signal transduction,” which gives the organism an “enhanced ability to sense and respond to conditions outside the cell” (11). It has both heterotrophic and lithoheterotrophic characteristics, which means that it relies on inorganic compounds such as carbon monoxide and sulfide for energy. S. pomeroyi has genes that are specialized in the uptake of compounds derived from algae, allow for fast growth, and facilitate the use of metabolites by the bacterium to reduce microzones. The Silicibacter genus is also known to possess numerous peptide transporters, which indicate the importance of proteins as carbon source for these species (11). Another distinctive feature of this bacterium is its six ABC-type transporter systems since “no other sequenced genome has more than three” (11). These transporter systems are likely to be used by S. pomeroyi for the purpose of cell growth regulation. S. pomeroyi also has five transport systems for DMSP transport, “four transporters for ammonium and one for urea” (11). Its genome houses genes that facilitate integration of ammonium and urea, which are useful sources of nitrogen (11).

In addition, the S. pomeroyi genome contains two cox operons that encode aerobic carbon monoxide dehydrogenases. These enzymes are used to oxidize carbon monoxide to carbone dioxide. There are also three rRNA operons present in the genome, which explains the organism’s ability to quickly respond to modifications depending on the availability of resources. When there is plenty of carbon and energy available, S. pomeroyi stores carbon and energy via the polyhydroxyalkanoic acid synthesis pathway. This organism does not display any evidence of pathways for autotrophy, which implies that it obtains its energy through carboxidotrophy, which is the process of utilizing carbon monoxide. The genome of S. pomeroyi also lacks genes that encode phototrophy (10). The genome contains “31 genes that encode elements for motility” (11). The organism achieves motility by rotating its complex flagellum (11). A growing body of evidence also suggests the presence of a large number of genes that encode “the production, degradation, and efflux of toxins and metabolites” (10) in marine organisms such as S. pomeroyi.

Cell structure and metabolism

Analysis of Silicibacter pomeroyi using different micrographs has allowed scientists to detect blebs (blisters) that are present in the outer membrane (5). These blebs may be responsible for the “degradation of insoluble substrates” (6). The bacterium also is seen to contain poly-β-hydroxybutyrate (PHB) inclusion bodies. The importance of the blebs and PHB bodies lies in the fact that they help Silicibacter pomeroyi to pick up and store nutrients, which allow them to survive in environments with low nutrient salt and high oxygen concentrations (5). This organism utilizes carbon monoxide as a source of energy (8). In addition, S. pomeroyi makes ATP for its energy needs. It has a respiratory sodium pump, which provides the sodium gradient necessary for ATP synthesis (10). S. pomeroyi uses organic acids, amino acids, and other compounds such as ethanol, glycerol, acetate, DMSP, glucose, pyruvate, and succinate (among other compounds) to grow at 10-40°C temperature range. S. pomeroyi requires NaCl for growth. Although vitamins are not required, enhanced growth is observed in their presence. S. pomeroyi is not able to either ferment glucose or reduce nitrate (5), but it can degrade aromatic compounds (1, 2). S. pomeroyi uses organic nitrogen and ammonium as sources of nitrogen. It can assimilate urea and ammonium (10). It hydrolyzes gelatin but not cellulose or starch. In the presence of arginine, S. pomeroyi can also oxidize thiosulfate. It has the capacity to produce both oxidase and catalase. It forms cream-colored, circular colonies on marine agar (5).

An important feature of S. pomeroyi is its ability to metabolize DMSP into DMS and MeSH using both the DMSP-cleavage and DMSP-demethylation/demethiolation pathways (9), respectivly. Only bacteria are known to have the capacity to utilize the demethylation/demethiolation pathway5.


Ecology

Silicibacter pomeroyi contributes to the environment by degrading DMSP to produce dimethylsulfide (DMS). DMS is a sulfur compound that makes a major contribution to the sulfur supply in the atmosphere. It also plays an important role in the regulation of the climate by forming clouds and scattering the radiation coming from the sun (3). Once in the atmosphere, DMS is oxidized to sulfuric acid and methanesulfonic acid. Both of these compounds have the ability to attract water molecules and condense them into clouds (7). The sulfur obtained from DMSP is integrated into proteins of bacteria; as a result, DMSP acts as a major source of sulfur for marine bacterioplankton (9). The ability to incorporate DMS sulfur into cell biomass is unique to organisms such as S. pomeroyi that are able to utilize the DMSP demethylation pathway (7). This organism has many mechanisms that allow it to sense and react to its environment as well as to obtain nutrients to facilitate growth. S. pomeroyi has three transporters that depend on sodium ions for activity. These transporters allow the organism to adapt to environments with high salt concentration. S. pomeroyi utilizies numerous ecologically important metabolic pathways such as DMSP demethylation and carbon monoxide oxidation among other pathways. This ability allows S. pomeroyi to adapt to various ecological environments (10).

Since S. pomeroyi belongs to the Roseobacter lineage, it is relevant to mention that members of the Roseobacter group interact with neighboring cells in an attempt to “increase their own access to resources” (10). It is also predicted that roseobacters may have the capacity to directly obtain organic substrates from eukaryotic cells. Members of the roseobacter group, including S. pomeroyi, utilize an ecological strategy that is important for surviv alin the surface of ocean waters. These organisms use their versatile cells to compete with other organisms for substrates (10).


Pathology

S. pomeroyi is not known to cause any diseases in humans, plants, or animals. It is an environmental microbe.

Current Research

1. “Investigating carbon monoxide (CO) consumption in the marine bacteria Silicibacter pomeroyi with coxL gene expression” (8).

This particular research focused on the consumption of carbon monoxide by marine bacteria such as S. pomeroyi. S. pomeroyi uses carbon monoxide as an energy source. The genome of this bacterium was studied to reveal two operons that encode the enzyme carbon monoxide dehydrogenase. This enzyme regulates the oxidation of carbon monoxide to carbon dioxide. The carbon monoxide dehydrogenase consists of several subunits. In this research, the large subunit coxL gene expression was examined at different concentrations of carbon monoxide. Gel electrophoresis was conducted, which depicted the production of bands of several of the coxL gene primers. These results implied that coxL is expressed constitutively by S. pomeroyi. coxL was expressed under all conditions, which means that carbon monoxide oxidation takes place continuously in marine waters independent of carbon monoxide concentration.

2. “Ecological Genomics of Marine Roseobacters” (10).

This paper attempts to answer three important questions pertaining to members of the roseobacter group. By studying the genome sequences of roseobacters, what physiological and ecological traits can be predicted? Which genes make roseobacters roseobacters? What genes are responsible for the marine characteristics of rosebacters? Three organisms belonging to the roseobacter group were examined, among which was S. pomeroyi. In response to the first questions, the studies revealed very important characteristics of S. pomeroyi, such as the existence of flagellum in S. pomeroyi, which gives the organism motility and thus allows it to place itself in heterogeneous environments that facilitate growth and survival. In addition, the researchers also found that Roseobacters posses ABC-type transporters as well as genes that encode up to six aerobic pathways which lead to the degradation of aromatic intermediates. To answer the second question, three transporters were discovered that allow roseobacters to adapt to high-salt environments. Roseobacters also have genes that facilitate extracellular signaling and degradation of aromatic compounds. The third question was answered by the evidence that forty genes were identified in S. pomeroyi which only appeared in other marine bacteria among which was the respiratory sodium pump which functions in ATP synthesis. Roseobacters make up a large portion of marine bacterioplankton communities.

3. “Silicibacter pomeroyi sp. nov. and Roseovarious nubinhibens sp. nov., dimethylsulfoniopropionate-demethylating bacteria from marine environments” (5).

This paper was written to describe the newly discovered Silicibacter pomeroyi. It talks about the physiological characteristics of the microbe and its functional abilities including the metabolic pathways that it utilizies. S. pomeroyi is a rod-shaped, Gram-negative cell belonging to the roseobacter lineage. An important component of the structure of this microbe is its complex flagellum. The flagellum contributes to its motility, which allows S. pomeroyi to place itself in favorable niches. The organisms has intracellulr poly-β-hydroxybutrate inclusions while its surface is covered with blebs (blisters filled with serous fluids) which contribute to the survival of S. pomeroyi in salt- and nutrient- deficient environments by facilitating the acquisition of nutrients. This organism has the capacity to degrade DMSP into DMS, an important source of atmospheric sulfur. In addition, a characteristic unique to S. pomeroyi is its ability to utilize the DMSP-demethylation/demethiolating pathway to produce MeSH, which facilitate the rapid incorporation of DMS-sulfur into bacterial proteins. Other relevant features of S. pomeroyi include its ability to oxidize carbon monoxide to carbon dioxide, growth at 10-40°C using ethanol, pyruvate, succinate, and glucose among other compounds, and inability to reduce nitrate or ferment glucose. This bacterium was isolated from coastal seawater in Georgia, USA. It plays an important role in the environment by regulating the climate among other things.

References

1. Buchan, A., Collier, L. S., Neidle, E. L. & Moran, M. A. “Key aromatic-ring-cleaving enzyme, protocatechuate 3,4-dioxygenase, in the ecologically important marine Roseobacter lineage.” Appl Environ Microbiol. 2000. Volume 66. p. 4662–4672. http://aem.asm.org/cgi/content/full/66/11/4662?view=long&pmid=11055908

2. Buchan, A., Neidle, E. L. & Moran, M. A. “Diversity of the ring-cleaving dioxygenase gene pcaH in a salt marsh bacterial community.” Appl Environ Microbiol. 2001. Volume 67. p. 5801–5809. http://aem.asm.org/cgi/content/full/67/12/5801?view=long&pmid=11722937

3. Charlson, R. J., Lovelock, J. E., Andreae, M. O. & Warren, S. G. “Oceanic phytoplankton, atmospheric sulfur, cloud albedo and climate.” Nature. 1987. Volume 326. p. 655–661.

4. Entrez Genome Project. http://www.ncbi.nlm.nih.gov/sites/entrez?db=genomeprj&cmd=Retrieve&dopt=Overview&list_uids=281

5. Gonzalez JM, Covert JS, Whitman WB, Henriksen JR, Mayer F, Scharf B, Schmitt R, Buchan A, Fuhrman JA, Kiene RP, Moran MA. “Silicibacter pomeroyi sp. nov. and Roseovarius nubinhibens sp. nov., dimethylsulfonioproprionate-demethylating bacteria from marine environments.” Int J Syst Evol Microbiol. 2003. Volume 53. p. 1261-9. http://ijs.sgmjournals.org/cgi/content/full/53/5/1261

6. Gonzalez, J. M. & Moran, M. A. “Numerical dominance of a group of marine bacteria in the a-subclass of the class Proteobacteria in coastal seawater.” Appl Environ Microbiol. 1997. Volume 63. p. 4237–4242. http://aem.asm.org/cgi/reprint/63/11/4237?view=long&pmid=9361410

7. González, J. M., Kiene, R. P. & Moran, M. A. “Transformation of sulfur compounds by an abundant lineage of marine bacteria in the -subclass of the class Proteobacteria.” Appl Environ Microbiol. 1999. Volume 65. p. 3810–3819. http://aem.asm.org/cgi/content/full/65/9/3810?view=long&pmid=10473380

8. Johnson, A., Moran, M. & Miller, W. “Investigating carbon monoxide (CO) consumption in the marine bacteria Silicibacter pomeroyi with coxL gene expression.” Geophysical Research Abstracts. 2007. Volume 9. p. 4535.

9. Kiene, R. P., Linn, L. J. & Bruton, J. A. “New and important roles for DMSP in marine microbial communities.” J Sea Res. 2000. Volume 43. p. 209–224.

10. Moran MA, Belas R., Schell M.A., Gonzalez J.M., Sun F., Sun S., Binder B.J., Edmonds J., Ye W., Orcutt B., Howard E.C., meile C., Palefsky W., Goesmann A., Ren Q., Paulsen L., Ulrich L.E., Thompson L.S., Saunders E., Buchan A. “Ecological genomics of marine roseobacters.” Appl. Environ. Microbiol. 2007. http://aem.asm.org/cgi/reprint/AEM.02580-06v1?view=long&pmid=17526795

11. Moran M.A., Buchan A., Gonzalez J.M., Heidelberg J.F., Whitman W.B., Kiene R.P., Henriksen J.R., King G.M., Belas R., Fuqua C., Brinkac L., Lewis M., Johri S., Weaver B., Pai G., Eisen J.A., Rahe E., Sheldon WM, Ye W., Miller T.R., Carlton J., Rasko D.A., Paulsen I.T., Ren Q., Daugherty S.C., Deboy R.T., Dodson R.J., Durkin A.S., Madupu R., Nelson W.C., Sullivan S.A., Rosovitz M.J., Haft D.H., Selengut J., Ward N. “Genome sequence of Silicibacter pomeroyi reveals adaptions to the marine environment.” Nature. 2004. Volume 432. p. 910-3. http://www.nature.com/nature/journal/v432/n7019/full/nature03170.html

12. Simó, R. “Production of atmospheric sulfur by oceanic plankton: biogeochemical, ecological and evolutionary links.” Trends Ecol Evol. 2001. Volume 16. p. 287–294. http://www.sciencedirect.com/science?_ob=ArticleURL&_udi=B6VJ1-430G202-W&_user=4429&_coverDate=06%2F01%2F2001&_rdoc=1&_fmt=&_orig=search&_sort=d&view=c&_acct=C000059602&_version=1&_urlVersion=0&_userid=4429&md5=7b9806fec1e036686335fb0835f759f8

13. Taxonomy Browser. http://www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi?mode=Info&id=89184&lvl=3&lin=f&keep=1&srchmode=1&unlock

Edited by Lusine Khachatryan, student of Rachel Larsen and Kit Pogliano

KMG