Characterization of Cyanobacterial Hydrocarbon Composition and Distribution of Biosynthetic Pathways

Abstract

Cyanobacteria possess the unique capacity to naturally produce hydrocarbons from fatty acids. Hydrocarbon compositions of thirty-two strains of cyanobacteria were characterized to reveal novel structural features and insights into hydrocarbon biosynthesis in cyanobacteria. This investigation revealed new double bond (2- and 3-heptadecene) and methyl group positions (3-, 4- and 5-methylheptadecane) for a variety of strains. Additionally, results from this study and literature reports indicate that hydrocarbon production is a universal phenomenon in cyanobacteria. All cyanobacteria possess the capacity to produce hydrocarbons from fatty acids yet not all accomplish this through the same metabolic pathway. One pathway comprises a two-step conversion of fatty acids first to fatty aldehydes and then alkanes that involves a fatty acyl ACP reductase (FAAR) and aldehyde deformylating oxygenase (ADO). The second involves a polyketide synthase (PKS) pathway that first elongates the acyl chain followed by decarboxylation to produce a terminal alkene (olefin synthase, OLS). Sixty-one strains possessing the FAAR/ADO pathway and twelve strains possessing the OLS pathway were newly identified through bioinformatic analyses. Strains possessing the OLS pathway formed a cohesive phylogenetic clade with the exception of three Moorea strains and Leptolyngbya sp. PCC 6406 which may have acquired the OLS pathway via horizontal gene transfer. Hydrocarbon pathways were identified in one-hundred-forty-two strains of cyanobacteria over a broad phylogenetic range and there were no instances where both the FAAR/ADO and the OLS pathways were found together in the same genome, suggesting an unknown selective pressure maintains one or the other pathway, but not both.

Contribution of cyanobacterial alkane production to the ocean hydrocarbon cycle

“…Total hydrocarbons in Synechococcus were between 0.304 and 2.580 fg per cell or 0.022-0.138% of dry cell weight (Table 1). With the exception of Prochlorococcus CCMP1986, which has the highest hydrocarbon yields so far observed in a cyanobacterium, hydrocarbon contents were within the range previously observed for other cyanobacteria (19).…”

“…The remainder consisted of 8-heptadecene. The hydrocarbon composition of Prochlorococcus and marine Synechococcus species differs from that of other alkaneproducing cyanobacteria, where heptadecane was the dominant hydrocarbon (19). The hydrocarbon composition of Synechococcus sp.…”

“…We first examined the genetic capability for hydrocarbon production in marine cyanobacterial genomes. Previous studies have demonstrated that hydrocarbon biosynthetic pathways are conserved in sequenced cyanobacteria, encompassing isolates from marine, freshwater, and terrestrial environments (19). This suggests that Significance A number of organisms synthesize hydrocarbons, but the scale at which this occurs in the environment is unknown.…”

“…With the exception of Leptolyngbya sp. PCC7376 and Moorea producens 3L, which encode Ols homologs, all of the other marine cyanobacteria including Cyanobium, Acaryochloris, Crocosphaera, Trichodesmium, Lyngbya, Oscillatoria, Nodularia, and Microcoleus species encode FAR/FAD homologs (15,19). Thus, it is likely that alkanes are the predominant hydrocarbons released by cyanobacteria into the marine environment.…”

“…Next, we measured the hydrocarbon contents of cultured Prochlorococcus and marine Synechococcus cells via gas chromatography-mass spectrometry (GC-MS). Hydrocarbon content has been quantified in a wide range of freshwater and terrestrial cyanobacteria, all of which produced either alkanes or alkenes, ranging between 0.024 and 0.262% of dry cell weight (19). However, the hydrocarbon content of Prochlorococcus and marine Synechococcus species has not been quantified.…”