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Edited by Edward F. DeLong, Massachusetts Institute of Technology, Cambridge, MA, and approved June 23, 2014 (received for review February 14, 2014)
Significance
The microbial community of the Amazon River Plume determines the fate of the world’s largest input of terrestrial carbon and nutrients to the ocean. By benchmarking with internal standards during sample collection, we determined that each liter of plume seawater contains 1 trillion genes and 50 billion transcripts from thousands of bacterial, archaeal, and eukaryotic taxa. Gene regulation by taxa inhabiting distinct microenvironments provides insights into micron-scale patterns of transformations in the marine carbon, nitrogen, phosphorus, and sulfur cycles in this globally important ecosystem.
Abstract
We investigated expression of genes mediating elemental cycling at the microspatial scale in the ocean’s largest river plume using, to our knowledge, the first fully quantitative inventory of genes and transcripts. The bacterial and archaeal communities associated with a phytoplankton bloom in Amazon River Plume waters at the outer continental shelf in June 2010 harbored ∼1.0 × 1013 genes and 4.7 × 1011 transcripts per liter that mapped to several thousand microbial genomes. Genomes from free-living cells were more abundant than those from particle-associated cells, and they generated more transcripts per liter for carbon fixation, heterotrophy, nitrogen and phosphorus uptake, and iron acquisition, although they had lower expression ratios (transcripts⋅gene−1) overall. Genomes from particle-associated cells contributed more transcripts for sulfur cycling, aromatic compound degradation, and the synthesis of biologically essential vitamins, with an overall twofold up-regulation of expression compared with free-living cells. Quantitatively, gene regulation differences were more important than genome abundance differences in explaining why microenvironment transcriptomes differed. Taxa contributing genomes to both free-living and particle-associated communities had up to 65% of their expressed genes regulated differently between the two, quantifying the extent of transcriptional plasticity in marine microbes in situ. In response to patchiness in carbon, nutrients, and light at the micrometer scale, Amazon Plume microbes regulated the expression of genes relevant to biogeochemical processes at the ecosystem scale.
Footnotes
- ↵1To whom correspondence should be addressed. Email: mmoran{at}uga.edu.
Author contributions: B.M.S., B.C.C., J.H.P., P.L.Y., and M.A.M. designed research; B.M.S., B.C.C., C.B.S., B.L.Z., M.D., and J.M. performed research; P.M.M. and V.J.C. contributed new reagents/analytic tools; B.M.S., B.C.C., C.B.S., S. Sharma, M.D., S. Sun, P.M.M., P.L.Y., and M.A.M. analyzed data; and B.M.S. and M.A.M. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in the Sequence Read Archive, www.ncbi.nlm.nih.gov/sra [accession nos. SRP039390 (metagenomes), SRP037995 (nonselective metatranscriptomes), and SRP039544 (poly(A)-selected metatranscriptomes)].
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1402782111/-/DCSupplemental.
- Brandon M. Satinskya,
- Byron C. Crumpb,
- Christa B. Smithc,
- Shalabh Sharmac,
- Brian L. Zielinskid,
- Mary Dohertye,
- Jun Mengc,
- Shulei Sunf,
- Patricia M. Medeirosc,
- John H. Pauld,
- Victoria J. Colese,
- Patricia L. Yagerc, and
- Mary Ann Moranc,1
- Departments of aMicrobiology and
- cMarine Sciences, University of Georgia, Athens, GA 30602;
- bCollege of Earth, Ocean, and Atmospheric Science, Oregon State University, Corvallis, OR 97331;
- dCollege of Marine Science, University of South Florida, St. Petersburg, FL 33701;
- eHorn Point Laboratory, University of Maryland Center for Environmental Science, Cambridge, MD 21613; and
- fCenter for Research in Biological Systems, University of California, San Diego, La Jolla, CA 92093
Edited by Edward F. DeLong, Massachusetts Institute of Technology, Cambridge, MA, and approved June 23, 2014 (received for review February 14, 2014)
Significance
The microbial community of the Amazon River Plume determines the fate of the world’s largest input of terrestrial carbon and nutrients to the ocean. By benchmarking with internal standards during sample collection, we determined that each liter of plume seawater contains 1 trillion genes and 50 billion transcripts from thousands of bacterial, archaeal, and eukaryotic taxa. Gene regulation by taxa inhabiting distinct microenvironments provides insights into micron-scale patterns of transformations in the marine carbon, nitrogen, phosphorus, and sulfur cycles in this globally important ecosystem.
Abstract
We investigated expression of genes mediating elemental cycling at the microspatial scale in the ocean’s largest river plume using, to our knowledge, the first fully quantitative inventory of genes and transcripts. The bacterial and archaeal communities associated with a phytoplankton bloom in Amazon River Plume waters at the outer continental shelf in June 2010 harbored ∼1.0 × 1013 genes and 4.7 × 1011 transcripts per liter that mapped to several thousand microbial genomes. Genomes from free-living cells were more abundant than those from particle-associated cells, and they generated more transcripts per liter for carbon fixation, heterotrophy, nitrogen and phosphorus uptake, and iron acquisition, although they had lower expression ratios (transcripts⋅gene−1) overall. Genomes from particle-associated cells contributed more transcripts for sulfur cycling, aromatic compound degradation, and the synthesis of biologically essential vitamins, with an overall twofold up-regulation of expression compared with free-living cells. Quantitatively, gene regulation differences were more important than genome abundance differences in explaining why microenvironment transcriptomes differed. Taxa contributing genomes to both free-living and particle-associated communities had up to 65% of their expressed genes regulated differently between the two, quantifying the extent of transcriptional plasticity in marine microbes in situ. In response to patchiness in carbon, nutrients, and light at the micrometer scale, Amazon Plume microbes regulated the expression of genes relevant to biogeochemical processes at the ecosystem scale.
- metatranscriptomics
- metagenomics
- biogeochemistry
- gene expression ratios
- marine bacteria
Footnotes
- ↵1To whom correspondence should be addressed. Email: mmoran{at}uga.edu.
Author contributions: B.M.S., B.C.C., J.H.P., P.L.Y., and M.A.M. designed research; B.M.S., B.C.C., C.B.S., B.L.Z., M.D., and J.M. performed research; P.M.M. and V.J.C. contributed new reagents/analytic tools; B.M.S., B.C.C., C.B.S., S. Sharma, M.D., S. Sun, P.M.M., P.L.Y., and M.A.M. analyzed data; and B.M.S. and M.A.M. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in the Sequence Read Archive, www.ncbi.nlm.nih.gov/sra [accession nos. SRP039390 (metagenomes), SRP037995 (nonselective metatranscriptomes), and SRP039544 (poly(A)-selected metatranscriptomes)].
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1402782111/-/DCSupplemental.
Gene expression in the Amazon River Plume
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