Overview
The general goal of the research in my lab is to advance our understanding of microbial ecology and evolution in the oceans. In recent years we have focused our attention on a single group, the cyanobacterium Prochlorococcus, which is the smallest and most abundant microbe in ocean ecosystems — sometimes accounting for half of the total chlorophyll. This “minimal phototroph” can convert CO₂, sunlight, and inorganic nutrients into a living cell with as few as 1700 genes.

We have been developing Prochlorococcus, and the phage that infect them, as a model system for understanding life processes across all scales of spatial and temporal organization, from the genome to the biosphere, and from daily to evolutionary time scales. In so doing, we hope to develop a unified understanding of this one small representative of the diversity of life.

Research Summary
Genome-enabled ecology of Prochlorococcus: Discovered only in the last two decades, Prochlorococcus is now known to be the most abundant photosynthetic cell in the oceans, often reaching 10⁸ cells L^-1. The cells are less than 1 micron in diameter, and are quite unusual for prokaryotes in that they contain divinyl chlorophylls a and b as their primary light-harvesting pigments. Their global abundance may be due in part to the existence of physiologically and genetically distinct “ecotypes” which, among other things, have different minimum, maximum, and optimal light intensities and temperatures for growth.

We now have the complete genome sequences of 12 Prochlorococcus strains, giving us a small window into the Prochlorococcus ‘pan-genome’, i.e., the total number of unique genes contained in all Prochlorococcus cells globally. The average genome size of a single isolate is about 2000 genes, 1100 of which are shared by all of the 12 isolates. Each new strain sequenced has contributed roughly 200 unique genes to the pan-genome thus far. With this small sample size, this increment shows no signs of diminishing as we add new genomes.

While all Prochlorococcus cells are very closely related phylogenetically (less than 3% difference in their 16S rRNA sequences), their whole genome sequences reveal both subtle and dramatic differences. The unshared genes among the strains that are most closely related are clustered in ‘islands’ of variability, for example, that appear to have dynamics facilitated by phage. Some of the genes that are unique to each ecotype have obvious roles in determining their relative fitness in the environments they dominate, while others do not. The latter hold clues to unknown agents of natural selection in the oceans, and we are eager to reveal their functions. We have recently developed the capability to sequence the genomes of single cells, which will significantly advance advance our understanding of the full diversity of ‘wild’ Prochlorococcus.

We are also studying Prochlorococcus as a model cell for advancing systems biology, through analysis of its transcriptome, proteome and regulatory network. Since the cell has a very small genome, is an autotroph, and has a very streamline regulatory system, it is a ‘minimal’ living unit.

At the other extreme of systems biology, we are studying the distribution and abundance of Prochlorococcus ecotypes, and their metagenomes and metatranscriptomes, in the global oceans to develop a framework for interpreting the evolution of their metabolic differences. We are analyzing their abundance as a function of time and depth at a station near Bermuda and a station near Hawaii, and use the Global Ocean Survey metagenomic dataset to better understand the global distribution of Prochlorococcus genes. Collectively, these analyses help us understand the origin and maintenance the diversity of the roughly 10²⁴ Prochlorococcus cells that occupy the world ocean.

Cyanophage: Phage are an integral part of the Prochlorococcus system. We have collected many lytic phage that infect Prochlorococcus from broad regions of the world oceans. We are studying phage/host specificity, and the infection dynamics of this system, and also undertaking a comparative genomics approach, using a growing number of phage genomes. All genomes examined thus far encode, transcribe, and translate host genes, including photosynthesis genes, suggesting that these genes are maintained by selection in the phage, and function to increase phage fitness, possibly by fortifying host metabolism during infection. Work is in progress to better understand how these genes function in the phage/host system, and contribute to niche differentiation in both host and phage. More fundamentally, we are interested in the role phage play in the evolution of ocean ecosystems.

To help develop Prochlorococcus as a model system, we have built a web site – a “Prochlorococcus Portal” – that summarizes genomic, transcriptomic, and proteomic data available for Prochlorocccus and its phage.

Professor Chisholm's areas of research interest are:

Microbiology

Ecology

Oceanography

Ecological Genomics

Selected Publications
Zinser, ER, D. Lindell, ZI Johnson, ME Futschik, C. Steglich, ML Coleman, MA Wright, T Rector, R Steen, N McNulty, LR Thompson, and SW Chisholm. 2009        Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, Prochlorococcus  PLoS ONE April 2009 | Volume 4 | Issue 4 | e5135

Frias-Lopez, J. Y. Shi, G. W. Tyson, M. L. Coleman, S.C. Schuster, S.W. Chisholm and E. F. DeLong. Microbial community gene expression in ocean surface waters. P.N.A.S. 105: 3805–3810 (2008).

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, Volume 3,Issue 12, e231: pp. 2515-2528 (2007).

Coleman, M.L. and S.W. Chisholm. Code and Context: Prochlorococcus as a model for cross-scale biology. Trends in Microbiology 15:398-407 (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. Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311:1737-1740. (2006).

Lindell, D, J. D. Jaffe, Z. I. Johnson, G. M. Church, S. W. Chisholm. Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438:86-89. (2005).

Sullivan, M.B., Coleman, M. Weigele, P. and Sallie W. Chisholm. Three Prochlorococcus cyanophage genomes: Signature features and ecological interpretations. PLoS Biology 3(5) e144:0001-0017. (2005).

Rocap G, Larimer F, Lamerdin J, Malfatti S, Chain P, Ahlgren N, Arellano A, Coleman M, Hauser L, Hess W, Johnson Z, Land M, Lindell D, Post A, Regala W, Shah M, Shaw S, Steglich C, Sullivan M, Ting C, Tolonen A, Webb E, Zinser E, Chisholm S. Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424: 1042-1047. (2003).

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