Characterization of Cyanobacterial Hydrocarbon Composition and Distribution of Biosynthetic Pathways

R Cameron Coates,Anton Korobeynikov,Pavel Pevzner,Sheila Podell,Alla Lapidus,David H Sherman,Eric E Allen,Lena Gerwick,William H Gerwick,Bing Xu

doi:10.1371/journal.pone.0085140

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.

Highlights

Cyanobacteria are a diverse group of photosynthetic bacteria that have evolved a remarkable array of adaptive traits including oxygenic photosynthesis, N2 fixation, a wide morphological diversity, extensive secondary metabolite biosynthetic capacity, and a range of symbiotic relationships with other organisms
A striking general conclusion that emerges from review of previous studies along with the results of this study is that hydrocarbon production is a universal phenomenon among cyanobacteria (Figure 2–4 and Table S1)
Heptadecane is the most commonly observed hydrocarbon in cyanobacteria followed by heptadecene, pentadecane and 7-methylheptadecane (Table S1) [2,5,44]

Summary

Introduction

Cyanobacteria are a diverse group of photosynthetic bacteria that have evolved a remarkable array of adaptive traits including oxygenic photosynthesis, N2 fixation, a wide morphological diversity, extensive secondary metabolite biosynthetic capacity, and a range of symbiotic relationships with other organisms. One trait less well characterized and potentially of great societal importance is their universal ability to produce long chain hydrocarbons. First recognition of this latter trait resulted from investigations in the 1960’s [2,3,4] and was of importance in the context of identifying the origin of hydrocarbons found in sedimentary and oil deposits. There has been a growing recognition of the negative environmental impacts of continued fossil fuel use, as well as an ever increasing worldwide energy demand, and these facts have combined to increase interest in developing sustainable biofuels such as hydrocarbons from cyanobacteria [5,6]. Many sources of renewable energy can be envisioned to help meet society’s demand for electrical power, there remains an acute need for low cost liquid fuels, and gasoline, diesel and jet fuel [6]

Methods

Results

Conclusion