From the Cover: Contribution of cyanobacterial alkane production to the ocean hydrocarbon cycle

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.Hydrocarbons are ubiquitous in the oceans, where natural seepage and human activities are estimated to release between 0.4 and 4.0 million tons of crude oil into the ocean ecosystem annually (1). Even in minimally polluted marine surface waters, alkanes such as pentadecane and heptadecane have been found at concentrations ranging from 2 to 130 pg/mL (2, 3), although their sources remain unclear. A small proportion of alkanes, from 1 to 60 fg/mL, is associated with particulate matter >0.7 µm in diameter (4). Larger amounts may be associated with particulate matter <0.7 µm in diameter, because ocean concentrations are higher than the solubility of pentadecane and heptadecane, which is ∼10 pg/mL and 1 pg/mL, respectively (2). Populations of hydrocarbon-degrading bacteria, referred to as hydrocarbonoclastic bacteria, including many species that cannot use other carbon sources, are present in marine systems and play an important role in turnover of these compounds (5–9). Because obligate hydrocarbon-degrading bacteria are found in waters without significant levels of crude oil pollution, these organisms must use an alternate hydrocarbon source (9–11).Here, we investigate the extent to which cyanobacteria may contribute to these marine hydrocarbon pools. Cyanobacteria (oxygenic photosynthetic bacteria) can synthesize C15 to C19 hydrocarbons via two separate pathways. The first produces alkanes, predominantly pentadecane, heptadecane, and methyl-heptadecane, in addition to smaller amounts of alkenes, via acyl-ACP reductase (FAR) and aldehyde deformylating oxygenase (FAD) enzymes (12). The second pathway generates alkenes, primarily nonadecene and 1,14-nonadecadiene, via a polyketide synthase enzyme (Ols) (13). The abundance and ubiquity of cyanobacteria in the marine environment suggests hydrocarbon production in the oceans could be considerable and broadly distributed geographically (14, 15).We focused our studies on the two most abundant marine cyanobacteria, Prochlorococcus and Synechococcus (16). These genera have estimated global population sizes of 2.9 ± 0.1 × 10²⁷ and 7.0 ± 0.3 × 10²⁶ cells, respectively (14), and are together responsible for approximately a quarter of marine net primary production (14). These are also the only cyanobacterial genera for which global population size estimates have been compiled (14). Although the distribution patterns of both genera overlap (14, 17), Prochlorococcus cells dominate low-nutrient open-ocean areas between 40°N and 40°S and can be found at depths of up to 200 m (16, 18). Synechococcus are more numerous in coastal and temperate regions where conditions and nutrient levels are more variable (14, 16) but are still widely distributed in high abundance.