Contribution of cyanobacterial alkane production to the ocean hydrocarbon cycle

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.cyanobacteria | hydrocarbons | hydrocarbon cycle | hydrocarbon-degrading bacteria | oil remediation

Hydrocarbons Are Essential for Optimal Cell Size, Division, and Growth of Cyanobacteria

“…Recently we demonstrated that 115 sequenced cyanobacteria isolated from a broad range of environments contain either the far/fad or ols genes, encoding the enzymes for alkane/alkene biosynthesis (Lea-Smith et al, 2015). In an additional 32 recently sequenced genomes from cyanobacteria, we found the same situation with the majority, 133/147, containing far/fad homologs (Supplemental Table S1).…”

“…For extraction of total hydrocarbons, 1.5 mL of dichloromethane was added to pelleted dried cells in glass vials, and hydrocarbons were extracted and analyzed by gas chromatography-mass spectrometry (GC-MS) according to Lea-Smith et al (2015). Hydrocarbons and lipids were extracted from Synechocystis thylakoid, cytoplasmic, and total membrane fractions, and Synechococcus total membrane fractions based on the method in Davey et al (2008) where 1 mL (3 mL for total membrane fractions) of chilled (220°C) solvent (methanol:chloroform:water, 2.5:1:1) was added to the membrane fraction tube, vortexed, and left in ice with occasional shaking.…”

“…All cyanobacteria with sequenced genomes encode the pathway for the biosynthesis of hydrocarbons, implying an important, although as-yet-undefined, role for these compounds (Lea-Smith et al, 2015). The major forms are C15-C19 alkanes and alkenes, which can be synthesized from fatty acyl-acyl-carrier proteins (ACPs) by one or other of two separate pathways ( Fig.…”

“…1; Schirmer et al, 2010;Mendez-Perez et al, 2011). The majority of species produce alkanes and alkenes via acyl-ACP reductase (FAR) and aldehyde deformylating oxygenase (FAD; Schirmer et al, 2010;Li et al, 2012;Coates et al, 2014;Lea-Smith et al, 2015). Cyanobacterial species lacking the FAR/FAD pathway synthesize alkenes via olefin synthase (Ols; Mendez-Perez et al, 2011;Coates et al, 2014;Lea-Smith et al, 2015).…”

“…Cyanobacterial hydrocarbons also have a significant environmental role. Due to the abundance of cyanobacteria in the environment, hydrocarbon production is considerable, with hundreds of millions of tons released into the ocean per annum following cell death (Lea-Smith et al, 2015). This production may be sufficient to sustain populations of hydrocarbon-degrading bacteria, which can then play an important role in consuming anthropogenic oil spills (Lea-Smith et al, 2015).…”