The overarching goal of my lab’s research is to advance our understanding of the ecology and evolution of microbes in the oceans, and how they influence global biogeochemical cycles. In recent years we have focused our attention on the cyanobacterium Prochlorococcus, which is the smallest and most abundant microbe in ocean ecosystems — sometimes accounting for half of the total photosynthetic biomass. This minimal phototroph can create a living cell with 1700 genes, sunlight, and inorganic compounds.
We are developing Prochlorococcus and its phage as a model system for studying life across all spatial scales, from genomes to the biosphere, and across evolutionary and generational time scales. We hope that by expanding systems biology across these dimensions for a single organisms, we will develop a more unified understanding of life processes.
Genome-enabled ecology of Prochlorococcus
Discovered only 25 years ago, the picocyanobacterium Prochlorococcus is the smallest and most abundant photosynthetic cell in the oceans, often reaching 108 cells L-1 with a global population of about 1027 cells. Their global abundance is due in part to the existence of physiologically and genetically distinct “ecotypes” which have different light and temperature optima for growth, and a myriad of other differences that provide opportunities for niche differentiation. All of this diversity is contained within a group that shares 97% similarity in rRNA sequence, and as such would be considered a single microbial species.
There is now a rich database of Prochlorococcus genomes from cultures, single cell genomes, and metagenomic databases. The average genome size is about 2000 genes, 1100 of which represent the core set of genes shared by all.Each new variant contributes roughly 200 unique genes to the global “pan-genome”, and the ‘distributed genome’ of Prochlorococcus globally is estimated at 57,000 genes. Many of the non-core genes in Prochlorococcus are clustered in genomic ‘islands’ acquired by horizontal gene transfer, sometimes bearing the signature of phage involvement.
We are also studying Prochlorococcus as a model cell for advancing systems biology, through analysis of its transcriptome, proteome and regulatory networks. Since the cell has a very small genome, is an autotroph, and has a very streamline regulatory system, it is a ‘minimal’ living unit simplifying analyses.
To unveil the selective pressures that have shaped the genetic diversity of Prochlorococcus, we study the distribution and abundance of Prochlorococcus ecotypes in the global oceans. Some of this work is focused on two study sites: a station near Bermuda and a station near Hawaii, and we use the Global Ocean Survey metagenomic dataset to better understand the biogeography of Prochlorococcus genes. Because the ocean environment is simple, and fluid, it offers a unique opportunity to study the relationship between genomic composition and environmental parameters. We are also involved in the NSF-Science and Technology Center C-MORE, which is dedicated to the study of the role of ocean microbes in global ocean processes.
Phage are an integral part of the Prochlorococcus system and we have isolated hundreds of phage that infect them from diverse ocean regions. Most phage genomes examined thus far encode, transcribe, and translate genes that have homologs in host cells — including photosynthesis genes. It appears that these genes function to increase phage fitness by augmenting bottlenecks in host metabolism during infection. They also serve as a reservoir of host genes in the global ocean, which is under a different set of selective pressures than when residing in a host genome.
To help develop Prochlorococcus as a model system for cross-scale biology, we have built a web site — a “Prochlorococcus Portal” — that hosts genomic, transcriptomic, proteomic, physiological, and biogeographical data available for Prochlorocccus and its phage.
Thompson, L. W. Q. Zeng, L. Kelly, K.H. Huang, S. U. Singer, J. Stubbe, and S. W. Chisholm. Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. PNAS 108(39) E757–E764. (2011)
Coleman, M. L. and S. W. Chisholm. Ecosystem-specific selection pressures revealed by comparative population genomics. PNAS 107 (43): 18634–18639 (2010).
Li, B. D. Sher, D, L. Kelly, Y. Shi, K. H. Huang, P.J. Knerr, I. Joewono, D. Rusch, S.W. Chisholm and W. van der Donk. Catalytic promiscuity in the biosynthesis of cyclic peptide secondary metabolites in planktonic marine cyanobacteria. PNAS 107(23) 10430-10435. (2010)
Kettler, G. A.C. Martiny, K. Huang, J. Zucker, M.L. Coleman, S. Rodrigue, F. Chen, A. Lapidus, S. Ferriera, J. Johnson, C. Steglich, G. Church, P. Richardson, S.W. Chisholm. Patterns and Implications of Gene Gain and Loss in the Evolution of Prochlorococcus. PLoS Genetics 3: 2515-2528 (2007).
Lindell, D. J.D. Jaffe, M.l. Coleman, I.M. Axmann, T. Rector, G. Kettler, M.B. Sullivan, R. Steen, W.R. Hess, G.M. Church, and S. W. Chisholm. Genome-wide expression dynamics of a marine virus and host reveal features of coevolution. Nature 449: 83-86 (2007).
Coleman, M.L., M.B. Sullivan, C. Steglich, E.F. DeLong and S.W. Chisholm. Genomic Islands and the ecology and evolution of Prochlorococcus. Science 311:1768-1770. (2006).
Johnson Z, Zinser ER, Coe A, McNulty NP, Woodward EMS, Chisholm SW. 2006. Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311:1737-1740. (2006).