Contribution of cyanobacterial alkane production to the ocean hydrocarbon cycle
- David J. Lea-Smitha,1,
- Steven J. Billerb,
- Matthew P. Daveyc,
- Charles A. R. Cottona,
- Blanca M. Perez Sepulvedad,
- Alexandra V. Turchyne,
- David J. Scanland,
- Alison G. Smithc,
- Sallie W. Chisholmb,f, and
- Christopher J. Howea
- aDepartment of Biochemistry, University of Cambridge, Cambridge CB2 1QW, United Kingdom;
- bDepartment of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139;
- cDepartment of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom;
- dSchool of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom;
- eDepartment of Earth Sciences, University of Cambridge, Cambridge CB2 3EQ, United Kingdom;
- fDepartment of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139
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Edited by John M. Hayes, Woods Hole Oceanographic Institution, Berkeley, CA, and approved September 8, 2015 (received for review April 14, 2015)
Significance
A number of organisms synthesize hydrocarbons, but the scale at which this occurs in the environment is unknown. Here, we provide the first global estimates of hydrocarbon production by the two most abundant cyanobacteria on Earth, Prochlorococcus and Synechococcus. We suggest that these organisms represent a significant and widespread source of hydrocarbons to the world’s oceans, which in turn may sustain populations of obligate hydrocarbon-degrading bacteria known to be important in consuming anthropogenic oil spills. Our study demonstrates the role cyanobacteria play in the ocean ‟hydrocarbon cycle” and reveals the massive scale of this process. The widespread distribution of cyanobacteria and hydrocarbon-degrading bacteria in freshwater, marine, and terrestrial environments suggests the hydrocarbon cycle is pervasive in many natural ecosystems.
Abstract
Hydrocarbons are ubiquitous in the ocean, where alkanes such as pentadecane and heptadecane can be found even in waters minimally polluted with crude oil. Populations of hydrocarbon-degrading bacteria, which are responsible for the turnover of these compounds, are also found throughout marine systems, including in unpolluted waters. These observations suggest the existence of an unknown and widespread source of hydrocarbons in the oceans. Here, we report that strains of the two most abundant marine cyanobacteria, Prochlorococcus and Synechococcus, produce and accumulate hydrocarbons, predominantly C15 and C17 alkanes, between 0.022 and 0.368% of dry cell weight. Based on global population sizes and turnover rates, we estimate that these species have the capacity to produce 2–540 pg alkanes per mL per day, which translates into a global ocean yield of ∼308–771 million tons of hydrocarbons annually. We also demonstrate that both obligate and facultative marine hydrocarbon-degrading bacteria can consume cyanobacterial alkanes, which likely prevents these hydrocarbons from accumulating in the environment. Our findings implicate cyanobacteria and hydrocarbon degraders as key players in a notable internal hydrocarbon cycle within the upper ocean, where alkanes are continually produced and subsequently consumed within days. Furthermore we show that cyanobacterial alkane production is likely sufficient to sustain populations of hydrocarbon-degrading bacteria, whose abundances can rapidly expand upon localized release of crude oil from natural seepage and human activities.
Footnotes
- ↵1To whom correspondence should be addressed. Email: djl63{at}cam.ac.uk.
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Author contributions: D.J.L.-S. and C.J.H. designed research; D.J.L.-S., S.J.B., M.P.D., and C.A.R.C. performed research; B.M.P.S. and D.J.S. contributed new reagents/analytic tools; D.J.L.-S., S.J.B., and M.P.D. analyzed data; and D.J.L.-S., S.J.B., M.P.D., C.A.R.C., B.M.P.S., A.V.T., D.J.S., A.G.S., S.W.C., and C.J.H. wrote the paper.
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The authors declare no conflict of interest.
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This article is a PNAS Direct Submission.
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See Commentary on page 13434.
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This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1507274112/-/DCSupplemental.



