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      Marine crude-oil biodegradation: a central role for interspecies interactions

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          Abstract

          The marine environment is highly susceptible to pollution by petroleum, and so it is important to understand how microorganisms degrade hydrocarbons, and thereby mitigate ecosystem damage. Our understanding about the ecology, physiology, biochemistry and genetics of oil-degrading bacteria and fungi has increased greatly in recent decades; however, individual populations of microbes do not function alone in nature. The diverse array of hydrocarbons present in crude oil requires resource partitioning by microbial populations, and microbial modification of oil components and the surrounding environment will lead to temporal succession. But even when just one type of hydrocarbon is present, a network of direct and indirect interactions within and between species is observed. In this review we consider competition for resources, but focus on some of the key cooperative interactions: consumption of metabolites, biosurfactant production, provision of oxygen and fixed nitrogen. The emphasis is largely on aerobic processes, and especially interactions between bacteria, fungi and microalgae. The self-construction of a functioning community is central to microbial success, and learning how such “microbial modules” interact will be pivotal to enhancing biotechnological processes, including the bioremediation of hydrocarbons.

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          Most cited references180

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          Microbial biosynthesis of alkanes.

          Alkanes, the major constituents of gasoline, diesel, and jet fuel, are naturally produced by diverse species; however, the genetics and biochemistry behind this biology have remained elusive. Here we describe the discovery of an alkane biosynthesis pathway from cyanobacteria. The pathway consists of an acyl-acyl carrier protein reductase and an aldehyde decarbonylase, which together convert intermediates of fatty acid metabolism to alkanes and alkenes. The aldehyde decarbonylase is related to the broadly functional nonheme diiron enzymes. Heterologous expression of the alkane operon in Escherichia coli leads to the production and secretion of C13 to C17 mixtures of alkanes and alkenes. These genes and enzymes can now be leveraged for the simple and direct conversion of renewable raw materials to fungible hydrocarbon fuels.
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            Algal-bacterial processes for the treatment of hazardous contaminants: a review.

            Microalgae enhance the removal of nutrients, organic contaminants, heavy metals, and pathogens from domestic wastewater and furnish an interesting raw material for the production of high-value chemicals (algae metabolites) or biogas. Photosynthetic oxygen production also reduces the need for external aeration, which is especially advantageous for the treatment of hazardous pollutants that must be biodegraded aerobically but might volatilize during mechanical aeration. Recent studies have therefore shown that when proper methods for algal selection and cultivation are used, it is possible to use microalgae to produce the O(2) required by acclimatized bacteria to biodegrade hazardous pollutants such as polycyclic aromatic hydrocarbons, phenolics, and organic solvents. Well-mixed photobioreactors with algal biomass recirculation are recommended to protect the microalgae from effluent toxicity and optimize light utilization efficiency. The optimum biomass concentration to maintain in the system depends mainly on the light intensity and the reactor configuration: At low light intensity, the biomass concentration should be optimized to avoid mutual shading and dark respiration whereas at high light intensity, a high biomass concentration can be useful to protect microalgae from light inhibition and optimize the light/dark cycle frequency. Photobioreactors can be designed as open (stabilization ponds or high rate algal ponds) or enclosed (tubular, flat plate) systems. The latter are generally costly to construct and operate but more efficient than open systems. The best configuration to select will depend on factors such as process safety, land cost, and biomass use. Biomass harvest remains a limitation but recent progresses have been made in the selection of flocculating strains, the application of bioflocculants, or the use of immobilized biomass systems.
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              Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter.

              We used a method that combines microautoradiography with hybridization of fluorescent rRNA-targeted oligonucleotide probes to whole cells (MICRO-FISH) to test the hypothesis that the relative contributions of various phylogenetic groups to the utilization of dissolved organic matter (DOM) depend solely on their relative abundance in the bacterial community. We found that utilization of even simple low-molecular-weight DOM components by bacteria differed across the major phylogenetic groups and often did not correlate with the relative abundance of these bacterial groups in estuarine and coastal environments. The Cytophaga-Flavobacter cluster was overrepresented in the portion of the assemblage consuming chitin, N-acetylglucosamine, and protein but was generally underrepresented in the assemblage consuming amino acids. The amino acid-consuming assemblage was usually dominated by the alpha subclass of the class Proteobacteria, although the representation of alpha-proteobacteria in the protein-consuming assemblages was about that expected from their relative abundance in the entire bacterial community. In our experiments, no phylogenetic group dominated the consumption of all DOM, suggesting that the participation of a diverse assemblage of bacteria is essential for the complete degradation of complex DOM in the oceans. These results also suggest that the role of aerobic heterotrophic bacteria in carbon cycling would be more accurately described by using three groups instead of the single bacterial compartment currently used in biogeochemical models.
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                Author and article information

                Journal
                Aquat Biosyst
                Aquat Biosyst
                Aquatic Biosystems
                BioMed Central
                2046-9063
                2012
                16 May 2012
                : 8
                : 10
                Affiliations
                [1 ]School of Biological Sciences, University of Essex, Wivenhoe Park, Colchester, CO4 3SQ, UK
                Article
                2046-9063-8-10
                10.1186/2046-9063-8-10
                3465203
                22591596
                ae0b3ad7-6589-43fd-abd5-ed7c5a14d6b1
                Copyright ©2012 McGenity et al.; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 6 February 2012
                : 25 April 2012
                Categories
                Review

                Ecology
                hydrocarbon,marine microbiology,biodegradation,alcanivorax,salt marsh,crude oil,biogeochemistry,microbial interactions,bioremediation

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