Pattern and synchrony of gene expression among sympatric marine microbial populations
Author(s)Ottesen, Elizabeth; Young III, Curtis Robert; Eppley, John Marmaduke; Ryan, John P.; Chavez, Francisco P.; Scholin, Christopher A.; DeLong, Edward; ... Show more Show less
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Planktonic marine microbes live in dynamic habitats that demand rapid sensing and response to periodic as well as stochastic environmental change. The kinetics, regularity, and specificity of microbial responses in situ, however, are not well-described. We report here simultaneous multitaxon genome-wide transcriptome profiling in a naturally occurring picoplankton community. An in situ robotic sampler using a Lagrangian sampling strategy enabled continuous tracking and repeated sampling of coherent microbial populations over 2 d. Subsequent RNA sequencing analyses yielded genome-wide transcriptome profiles of eukaryotic (Ostreococcus) and bacterial (Synechococcus) photosynthetic picoplankton as well as proteorhodopsin-containing heterotrophs, including Pelagibacter, SAR86-cluster Gammaproteobacteria, and marine Euryarchaea. The photosynthetic picoplankton exhibited strong diel rhythms over thousands of gene transcripts that were remarkably consistent with diel cycling observed in laboratory pure cultures. In contrast, the heterotrophs did not cycle diurnally. Instead, heterotrophic picoplankton populations exhibited cross-species synchronous, tightly regulated, temporally variable patterns of gene expression for many genes, particularly those genes associated with growth and nutrient acquisition. This multitaxon, population-wide gene regulation seemed to reflect sporadic, short-term, reversible responses to high-frequency environmental variability. Although the timing of the environmental responses among different heterotrophic species seemed synchronous, the specific metabolic genes that were expressed varied from taxon to taxon. In aggregate, these results provide insights into the kinetics, diversity, and functional patterns of microbial community response to environmental change. Our results also suggest a means by which complex multispecies metabolic processes could be coordinated, facilitating the regulation of matter and energy processing in a dynamically changing environment.
DepartmentMassachusetts Institute of Technology. Department of Biological Engineering; Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
Proceedings of the National Academy of Sciences of the United States of America
National Academy of Sciences (U.S.)
Ottesen, E. A., C. R. Young, J. M. Eppley, J. P. Ryan, F. P. Chavez, C. A. Scholin, and E. F. DeLong. “PNAS Plus: Pattern and synchrony of gene expression among sympatric marine microbial populations.” Proceedings of the National Academy of Sciences 110, no. 6 (February 5, 2013): E488-E497.
Final published version