Stephen Giovannoni
Marine Microbial Ecology, Physiology and Genomics
Research Interests: Genome evolution and metabolism of the marine bacterium SAR11, the marine carbon cycle, high throughput microbial culturing, proteomics, metabolomics
Office: 248 Nash Hall
Courses taught:
MB 420/520 Microbial Diversity, MB/MCB 668/669 Bioinformatics and Genomics, MCB 669 Genome Evolution
Degrees: Ph.D. University of Oregon
RESEARCH
Our goal is to understand how dominant marine bacteria function in global biogeochemical cycles. We are particularly interested in the carbon cycle and SAR11, one of the smallest and most abundant organisms on the planet.
We made the strategic decision to focus on pure cultures of marine bacteria that can be studied in a controlled laboratory setting. We use metagenomics and oceanographic field work to link laboratory discoveries to natural processes. The work described below was made possible by the success of OSU's High Throughput Culturing Laboratory (HTCL), a facility we developed to isolate and study bacteria at the extremely low nutrient concentrations found in many natural environments.
Our work is supported by the Marine Microbiology Initiative of the Gordon and Betty Moore Foundation and the National Science Foundation.
Genome Streamlining. Studies of SAR11 and another marine bacterium, OM43, have led us to the surprising conclusion that metabolic versatility has been sacrificed for simplicity and small genome size in some bacterioplankton, rendering them able to use ambient nutrient resources efficiently but reducing their metabolic versatility. Most of our research is focused on SAR11 isolates called Pelagibacter. Pelagibacter genomes (1.31 - 1.46 Mbp) are the smallest reported for free-living heterotrophic cells. The essence of the genome streamlining theory is that evolutionary selection is efficient at eliminating unnecessary DNA from very large, successful microbial populations. Recently, extraordinary examples of genome reduction in SAR11 emerged. These cells are deficient in assimilatory sulphate reduction genes, making them dependent on exogenous sources of reduced sulphur, such as 3-dimethyl- sulphoniopropionate (DMSP) or methionine, for growth. We also found that SAR11 cells are glycine auxotrophs that use a unique and elegantly simple glycine-activated riboswitch on malate synthase to control the assimilation of carbon through the TCA cycle into biomass.
Sargasso Sea Microbial Observatory. We collaborate with oceanographer Dr. Craig Carlson in this long-term NSF-sponsored project that takes an ecological perspective to understanding the role of microorganisms in the oceanic carbon cycle. Our study site in the Western Sargasso Sea (a.k.a. BATS, the Bermuda Atlantic Time-series Study) is an example of an oligotrophic ocean gyre. Seventy percent of the oceans are gyres, regions of clear water and low productivity. At BATS we use a variety of experimental approaches, including metagenomics, metaproteomics, fluorescence in situ hybridization and chemical measurements, to understand how microbial communities recycle organic matter.
Environmental Proteomics. Mass spectrometry can identify proteins extracted from complex microbial communities, revealing the endpoints of transcription and translation - the proteomes of cells. To study the mechanisms of microbial survival in oligotrophic oceans, we work with Drs. Mary Lipton and Richard Smith of Pacific Northwest National Laboratory and Dr. Doug Barofsky of OSU, applying capillary LC-tandem mass spectrometry to detect microbial proteins in samples collected from seawater. We have found that mass spectra from periplasmic substrate-binding proteins account for a disproportionately large fraction of the bacterial proteins in seawater, consistent with models that predict streamlining selection and high surface to volume ratios in oligotrophic bacterioplankton. At our study site in the Sargasso Sea, the most abundant SAR11 peptides are from periplasmic substrate-binding proteins for phosphate, amino acids, phosphonate, sugars, and spermidine.
Environmental Metabolomics. Marine dissolved organic matter (DOM) has so far eluded comprehensive chemical description, veiling complex interactions between abiotic and biotic processes that control this vast pool of reactive carbon. Working with Dr. Elizabeth Kujawinski of Woods Hole Oceanographic Institution and Dr. Sam Bennett of OSU, we are developing applications of mass spectrometry to study DOM composition. This ongoing research is identifying specific metabolic strategies used by marine bacteria to oxidize marine DOM.
The High Throughput Cultivation Laboratory (HTCL). One of our major activities is the culturing of new microbial species from the oceans and the sequencing and analysis of genomes from these strains. We also maintain a culture collection that distributes these strains and their DNA to other investigators. Our earlier research on applications of molecular biology to microbial ecology helped establish the broad and fundamental observation that a majority of the microorganisms in natural ecosystems have not been cultured in scientific laboratories. Understanding these organisms is critical to the development of local and global geochemical models, as well as socially relevant issues such as bioremediation. They are also a major reservoir of natural diversity that is yielding new enzymes and small molecules for the chemical industry, agriculture, and medicine. OSU's HTCL addresses this problem with robotics, flow cytometry and cell arraying techniques that enable us to culture and identify cells at the very low growth rates and nutrient concentrations that are typical of natural ecosystems.
SELECTED PUBLICATIONS
Pub Med
Carlson, C.A., R. Morris, R. Parsons, A. H. Treusch, S.J. Giovannoni, K. Vergin. 2009. Seasonal patterns in SAR11 populations in the euphotic and mesopelagic zones of the Northwestern Sargasso Sea. ISME J. Epub ahead of print.
Tripp, H. J., M. S. Schwalbach, M.S., M .M. Meyer, J. B. Kitner, R. R. Breaker and S. J. Giovannoni. 2009. Unique glycine-activated riboswitch linked to glycine-serine auxotrophy in SAR11. Environ. Microbiol. 11:230-238.
Sowell, S.M., L. J. Wilhelm, A. D. Norbeck, M. S. Lipton, C. Nicora, D. F. Barofsky, C. A. Carlson, R. D. Smith, S. J. Giovanonni. 2008 Transport functions dominate the SAR11 metaproteome at low nutrient extremes in the Sargasso Sea. 74(13):4091-100.
Giovannoni, S. J., D. H. Hayakawa, H. J. Tripp, U. Stingl, S. Givan, J.-C. Cho, H.-M. Oh, J. B. Kitner, K. L. Vergin, and M. S. Rappé. 2008. The small genome of an abundant coastal ocean methylotroph. Environ. Microbiol. 10:1771-82.
Tripp, H. J., J. B. Kitner, M. S. Schwalbach, J. W. H. Dacey, L. J. Wilhelm, and S. J. Giovannoni. 2008. SAR11 marine bacteria require exogenous reduced sulphur for growth. Nature 452: 741-744.
Wilhelm, L., S. H. J. Tripp, S. Givan, D. Smith and S. J. Giovannoni. 2007. Natural variation in SAR11 marine bacterioplankton genomes inferred from metagenomic data. Biol. Direct. 2:27 doi:10.1186/1745-6150-2-27.
Giovannoni, S. J., H. J. Tripp, S. Givan, M. Podar, K. L. Vergin, D. Baptista, L. Bibbs, J. Eads, T. H. Richardson, M. Noordewier, M. S. Rappé, J. Short, J. C. Carrington and E. J. Mathur. 2005. Genome streamlining in a cosmopolitan oceanic bacterium. Science 309:1242-1245.
Giovannoni, S. J., L. Bibbs, J. C. Cho, M. D. Stapels, R. Desiderio, K. L. Vergin, M. S. Rappé, S. Laney, L. Wilhelm, H. J. Tripp, E. J. Mathur and D. F. Barofsky. 2005. Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 483:82-85
Morris, R.M., M. S. Rappé, S. A. Connon, K. L. Vergin, W. A. Siebold, C.A. Carlson, S. J. Giovannoni. 2002. High cellular abundance of the SAR11 bacterioplankton clade in seawater. Nature 420:806-810.
Rappé, M.S , S. Connon, S., K. L. Vergin, and S. J. Giovannoni. 2002. Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418:630-631.
Giovannoni, S.J., M. S. Rappé, K. L. Vergin and N. Adair. 1996. 16S rRNA genes reveal stratified open ocean bacterioplankton populations related to the Green Non-Sulfur bacteria. Proc. Natl. Acad. Sci. U.S.A . 93:7979-7984.
Suzuki, M., and S. J. Giovannoni. 1996. Bias caused by template annealing in the amplification of 16S rRNA genes by PCR. Appl. Environ. Microbiol . 62:625-630.
Giovannoni, S. J., T. B. Britschgi, C. L. Moyer, and K. G. Field. 1990. Genetic diversity in Sargasso Sea bacterioplankton. Nature 345:60-63.