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The Official Magazine of the Oceanography Society OceTHE OFFICIALa MAGAZINEn ogOF THE OCEANOGRAPHYra SOCIETYphy CITATION Joye, S.B., S. Kleindienst, J.A. Gilbert, K.M. Handley, P. Weisenhorn, W.A. Overholt, and J.E. Kostka. 2016. Responses of microbial communities to hydrocarbon exposures. Oceanography 29(3):136–149, http://dx.doi.org/10.5670/oceanog.2016.78. DOI http://dx.doi.org/10.5670/oceanog.2016.78 COPYRIGHT This article has been published in Oceanography, Volume 29, Number 3, a quarterly journal of The Oceanography Society. Copyright 2016 by The Oceanography Society. All rights reserved. USAGE Permission is granted to copy this article for use in teaching and research. Republication, systematic reproduction, or collective redistribution of any portion of this article by photocopy machine, reposting, or other means is permitted only with the approval of The Oceanography Society. Send all correspondence to: [email protected] or The Oceanography Society, PO Box 1931, Rockville, MD 20849-1931, USA. DOWNLOADED FROM HTTP://TOS.ORG/OCEANOGRAPHY GoMRI: DEEPWATER HORIZON OIL SPILL AND ECOSYSTEM SCIENCE Responses of Microbial Communities to Hydrocarbon Exposures By Samantha B. Joye, Sara Kleindienst, Jack A. Gilbert, Kim M. Handley, Pam Weisenhorn, Will A. Overholt, and Joel E. Kostka 136 Oceanography | Vol.29, No.3 The impact of hydrocarbon pollution on the composition, structure, and function of microbial communities is evident in the responses“ of taxa able to use hydrocarbons as sources of carbon and energy.”. ABSTRACT. The responses of microbial communities to hydrocarbon exposures are natural gas to the deep waters (~1,500 m) complex and variable, driven to a large extent by the nature of hydrocarbon infusion, of the Gulf of Mexico (Joye, 2015). Some local environmental conditions, and factors that regulate microbial physiology seven million liters of chemical disper- (e.g., substrate and nutrient availability). Although present at low abundance in the ocean, sants, mainly Corexit 9500 and 9527A, hydrocarbon-degrading seed populations are widely distributed, and they respond were applied as a response measure at the rapidly to hydrocarbon inputs at natural and anthropogenic sources. Microbiomes sea surface and at the discharging well- from environments impacted by hydrocarbon discharge may appear similar at a head. Of the discharged oil and gas, all of higher taxonomic rank (e.g., genus level) but diverge at increasing phylogenetic the low molecular weight alkanes (meth- resolution (e.g., sub-OTU [operational taxonomic unit] levels). Such subtle changes are ane through propane) and half of the dis- detectable by computational methods such as oligotyping or by genome reconstruction charged oil were entrained in a deep- from metagenomic sequence data. The ability to reconstruct these genomes, and water plume at a depth of approximately to characterize their transcriptional activities in different environmental contexts 1,000 m (Joye, 2015). The microbial through metatranscriptomic mapping, is revolutionizing our ability to understand the response to this hydrocarbon infusion, diverse and adaptable microbial communities in marine ecosystems. Our knowledge especially at low deep-ocean tempera- of the environmental factors that regulate microbial hydrocarbon degradation and tures, was swift and remarkable (Joye the efficiency with which marine hydrocarbon-degrading microbial communities et al., 2014; Kleindienst et al., 2015a). bioremediate hydrocarbon contamination is incomplete. Moreover, detailed baseline Oil is a mixture of hydrocarbons, descriptions of naturally occurring hydrocarbon-degrading microbial communities which are organic molecules consisting and a more robust understanding of the factors that regulate their activity are needed. of carbon atoms bonded to each other and to hydrogen atoms. Some com- INTRODUCTION water hydrocarbon discharge to date. On plex hydrocarbons contain nitrogen and Oil is introduced into the marine envi- April 20, 2010, operators lost well con- sulfur residues (Seidel et al., 2016), as well ronment through natural seepage and trol on the DWH mobile offshore drilling as metalloids; oxygen is introduced into as a result of human activities, includ- unit. A subsequent gas-fueled explosion hydrocarbons during biodegradation ing pipeline and tanker leaks and spills, resulted in the sinking of the platform and weathering (Aeppli et al., 2012). The for example, the Exxon Valdez oil spill in two days later. Upon sinking, the riser major hydrocarbon classes include sat- 1989, and in some cases large acciden- pipe separated from the drilling platform, urates (e.g., linear, branched, and cyclic tal ocean discharges, for example, the generating an uncontrolled oil well blow- alkanes), aromatics (where single and Ixtoc blowout in the southern Gulf of out at the seafloor. double bonds exist and help to stabilize Mexico in 1979 and the BP/Deepwater The DWH well blowout discharged the compound), resins, and asphaltenes. Horizon (DWH) discharge in 2010, approximately five million barrels of oil A number of aromatic hydrocarbons which ranks as the largest marine open and at least 250,000 metric tonnes of are toxic, making it pragmatic to Oceanography | September 2016 137 understand the potential of microbial impacts (Figure 1). Microbial hydro- anaerobic pathways are more novel and populations to moderate the impacts of carbon degradation occurs under oxic, complex (Widdel et al., 2010). hydrocarbon pollution. Identifying the microaerophilic, and anoxic conditions The impact of hydrocarbon pollution microorganisms responsible for oil bio- (Head et al., 2003). Complete hydro- on the composition, structure, and func- degradation and understanding the fac- carbon oxidation is achieved though tion of microbial communities is evident tors that regulate bioremediation in the the collective action of associated, inter- in the responses of taxa able to use hydro- marine environment is critical. dependent microorganisms. Though the carbons as sources of carbon and energy. The ability to degrade hydrocarbons metabolic pathways of hydrocarbon oxi- Many of these organisms exist as part of is widespread among the bacteria, meth- dation are similar at the genus level, pri- the “rare biosphere,” a “seed bank” of taxa anogenic archaea, and fungi (Leahy and mary pathways are linked to more taxo- (Gibbons et al., 2013) that are ecologically Colwell, 1990; Head et al., 2003, 2006). nomically diverse secondary pathways noncompetitive, except when exposed to These microorganisms degrade oil (Heider and Rabus, 2008). Aerobic bio- hydrocarbons (Kleindienst et al., 2015a). and gas, either partially or completely, degradation has received more atten- Spatiotemporal investigations of micro- and reduce negative environmental tion than anaerobic biodegradation, but bial community responses to oil pollu- tion revealed the influence that blooms of conditionally rare, opportunistic taxa Biological network of oil, dispersed oil, and dispersant degradaon have on community structure and func- tion (Lu et al., 2012; Mason et al., 2012; Fe Kleindienst et al., 2015a). Subsequent Nutrients N P studies explored how community changes altered the broader ecological proper- ties of polluted environments; for exam- Biologically ple, metagenomic analysis of oil-polluted Bio- dispersed sediments showed that their microbial oil Chemical surfactant dispersants communities had an elevated potential for anaerobic ammonium oxidation, or anammox (Scott et al., 2014). Large-scale hydrocarbon inputs stim- ulate oxygen consumption as a conse- quence of accelerated aerobic microbial activity. When oxygen is depleted, anaer- Chemically obic hydrocarbon metabolism is coupled dispersed oil to sulfate and nitrate reduction, which fundamentally shifts the nitrogen, sulfur, and carbon cycles, and promotes further changes in microbial structure and com- Metabolic Metabolic position as a function of breakdown prod- products products ucts and cross-feeding (Kleindienst et al., 2015b). After hydrocarbon exposure, the Grazers Viruses community may return to its original eco- logical functional state or be altered, with certain taxa increasing in abundance fol- lowing hydrocarbon bioremediation and persisting on a time scale of years post- FIGURE 1. Biological network of oil, dispersed oil, and dispersant degradation. disturbance (Kleindienst et al., 2015a). Hydrocarbon-oxidizing microbes with the capability to produce biosurfactants to In this article, we describe the path- facilitate oil degradation are shown in blue. It remains a question as to whether ways of hydrocarbon degradation in the the activity of these microorganisms is stimulated or inhibited by chemical disper- sants. Different types of hydrocarbon degraders, shown in red, have the ability to environment, the methods used to quan- degrade chemically dispersed oil as well as dispersants (e.g., Colwellia sp. RC25). tify hydrocarbon degradation rates and Secondary metabolite consumers of compounds produced during oil biodegrada- the microorganisms that mediate these tion, for which dispersant impacts are largely unknown, are shown in gray. Parts of this network (nutrient availability, viruses, and grazers) likely influence all the above reactions, and how microbial populations types of microorganisms. Illustration based on Head et al. (2006) respond to hydrocarbon inputs. 138 Oceanography | Vol.29, No.3 PATHWAYS OF HYDROCARBON Aerobic Degradation groups of metalloenzymes, particulate DEGRADATION The aerobic degradation of alkanes, par- methane monooxygenase
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