Pattern and synchrony of gene expression among sympatric marine microbial populations
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-...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | en_US |
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National Academy of Sciences (U.S.)
2013
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| Online Access: | http://hdl.handle.net/1721.1/80761 |
| _version_ | 1826214134955376640 |
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| author | Ottesen, Elizabeth Young III, Curtis Robert Eppley, John Marmaduke Ryan, John P. Chavez, Francisco P. Scholin, Christopher A. DeLong, Edward |
| author2 | Massachusetts Institute of Technology. Department of Biological Engineering |
| author_facet | Massachusetts Institute of Technology. Department of Biological Engineering Ottesen, Elizabeth Young III, Curtis Robert Eppley, John Marmaduke Ryan, John P. Chavez, Francisco P. Scholin, Christopher A. DeLong, Edward |
| author_sort | Ottesen, Elizabeth |
| collection | MIT |
| description | 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. |
| first_indexed | 2024-09-23T16:00:02Z |
| format | Article |
| id | mit-1721.1/80761 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T16:00:02Z |
| publishDate | 2013 |
| publisher | National Academy of Sciences (U.S.) |
| record_format | dspace |
| spelling | mit-1721.1/807612022-10-02T05:39:30Z Pattern and synchrony of gene expression among sympatric marine microbial populations Ottesen, Elizabeth Young III, Curtis Robert Eppley, John Marmaduke Ryan, John P. Chavez, Francisco P. Scholin, Christopher A. DeLong, Edward Massachusetts Institute of Technology. Department of Biological Engineering Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Ottesen, Elizabeth Young III, Curtis Robert Eppley, John Marmaduke DeLong, Edward 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. National Science Foundation (U.S.) (Science and Technology Center Award EF0424599) Gordon and Betty Moore Foundation Agouron Institute David & Lucile Packard Foundation 2013-09-16T19:48:31Z 2013-09-16T19:48:31Z 2013-01 2012-12 Article http://purl.org/eprint/type/JournalArticle 0027-8424 1091-6490 http://hdl.handle.net/1721.1/80761 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. en_US http://dx.doi.org/10.1073/pnas.1222099110 Proceedings of the National Academy of Sciences of the United States of America Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf National Academy of Sciences (U.S.) PNAS |
| spellingShingle | Ottesen, Elizabeth Young III, Curtis Robert Eppley, John Marmaduke Ryan, John P. Chavez, Francisco P. Scholin, Christopher A. DeLong, Edward Pattern and synchrony of gene expression among sympatric marine microbial populations |
| title | Pattern and synchrony of gene expression among sympatric marine microbial populations |
| title_full | Pattern and synchrony of gene expression among sympatric marine microbial populations |
| title_fullStr | Pattern and synchrony of gene expression among sympatric marine microbial populations |
| title_full_unstemmed | Pattern and synchrony of gene expression among sympatric marine microbial populations |
| title_short | Pattern and synchrony of gene expression among sympatric marine microbial populations |
| title_sort | pattern and synchrony of gene expression among sympatric marine microbial populations |
| url | http://hdl.handle.net/1721.1/80761 |
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