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3-25-2020

Deepwater Horizon and the Rise of the Omics

Joel E. Kostka Georgia Institute of Technology

Samantha Joye University of Georgia

Rita Collwell University of Maryland

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Scholar Commons Citation Kostka, Joel E.; Joye, Samantha; and Collwell, Rita, "Deepwater Horizon and the Rise of the Omics" (2020). C-IMAGE Publications. 6. https://scholarcommons.usf.edu/cimage_pubs/6

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28 Eos // april 2020 DEEPWATER HORIZON AND THE RISE OF THE

Microbial genomics techniques came of age following the Deepwater Horizon spill, offering researchers MICSunparalleled insights into how ecosystems respond to such environmental disasters.

By Joel E. Kostka, Samantha Joye, and Rita Colwell

Photograph of oil beneath the surface of the Gulf of Mexico following the Deepwater Horizon spill (background). In the inset, microscopic speci- mens of Candidatus Macondimonas diazotrophica are visible both inside and around the edges of oil droplets (large round shapes) in this micro- scope image. Credits: Rich Matthews/AP images (photo); Shutterstock/CoreDESIGN (DNA illustration); and Shmruti Karthikeyan (inset)

SCIENCE NEWS BY AGU // Eos.org 29 lmost everywhere scientists gas) that enters the marine environment The DWH spill have looked on or near through natural mechanisms like seeps was also the first Earth’s surface—from ­ice-​ [Leahy and Colwell, 1990]. major environ- ­buried Antarctic lakes to As researchers began unveiling the com- mental disaster for arid, ­ultraviolet-​­baked des- plexity of microbial communities and illu- which genomics erts and ecosystems ranging minated fundamentals of how they operate technologies had from pristine to heavily polluted—they have in recent decades, though, much remained matured to such Afound abundant and often highly diverse unclear about their structure and function- an extent that they populations of microorganisms. Microor- ing in nature. The reason for this was in part could be deployed ganisms, or microbes, are everywhere; they because of a shortage of techniques for to quantify micro- are adaptable, and they play key roles in ele- studying them. Because of their small size, bial responses ment cycling and ecosystem functioning in microbes evade easy observation, and most over large spatial nearly every environment on Earth. cannot be cultured in the laboratory. At the and temporal Microbes are the great decomposers in time of the Exxon Valdez oil spill in 1989, for scales. As a result, ecosystems, breaking down dead and dying example, environmental microbiology was a the field of envi- organic matter and recycling major nutrients relatively nascent field. But in the past ronmental for use by plants. And by reacting rapidly and decade, a variety of ­so-​­called omics tech- genomics matured adapting to changing conditions, they act as niques, focused on parsing the genetic during the past first responders in helping restore balance makeup of cells, have emerged and offered decade in parallel and stability to ecosystems after such distur- researchers powerful new ways to study with the DWH bances as pollution or catastrophic storms. microbial communities and the roles played response. Techni- Microbes are, for example, intimately by specific groups of microbes. cal advances in involved in ecosystem responses to oil spills. genomics enabled Like organic matter derived from Omics Emerge direct, compre- modern-­ day​­ primary production, oil The 2010 Deepwater Horizon (DWH) oil spill hensive analyses formed over geologic time can act as a car- in the Gulf of Mexico is the largest acciden- of the microbes in bon source that fuels microbial growth and tal oil discharge into a marine environment their natural habi- metabolism. Hydrocarbon-­ degrading​­ for which a proportional emergency tat, be it ­oil-​­contaminated or uncontami- microbes have been studied for decades response effort was mounted. In contrast to nated seawater or sediments. Researchers and are thought to be ubiquitous and the Valdez spill, the last major spill affect- studying the effects of the DWH spill pre- diverse and to have adapted to consuming ing the United States before 2010, the DWH sided over an explosion of microbial oil over millions of years [Head et al., 2006]. discharge occurred in deep water, with genomics data that enabled major advances And biodegradation mediated by indige- extraordinarily large volumes of chemical in oil spill science and allowed scientists to nous microbial communities is considered dispersant applied during emergency answer the question, What microbes are the primary fate of most petroleum (oil and response efforts. there?, in complex communities in unprec- edented detail. Metagenomics, the sequencing of all genes for all organisms in a sample, enabled determinations of the full range of micro- bial species present. It also provided assess- ments of these organisms’ metabolic potential to carry out important ecosystem processes like photosynthesis and the deg- radation of certain carbon compounds. Application of metatranscriptomics, the sequencing of active or expressed genes, provided opportunities to decipher the functions or activities of those same microbes in nature, essentially answering the question, What are they doing? Gene sequences are collected from the environment in fragments. Recent improvements in bioinformatics tools, which use ­high-performance​­ computing to stitch these fragments back together into the genomes of individual microbial spe- This sand core (left) collected on 30 June 2010 at Pensacola Beach, Fla., contains a pronounced oiled layer cies, have allowed scientists to reconstruct (dark brown). More than 50% of the microbes in that layer belonged to genus Marinobacter (in the Alteromonad- microbial genomes over large scales, reveal- ales order), a known hydrocarbon-degrading microbial group, far more than in sands below and above the oiled ing the incredible diversity and complexity layer. Credit: Markus Huettel of microbial communities.

30 Eos // april 2020 scientific partner- et al., 2011; Yang et al., 2016; Kleindienst et al., ships enabled 2015]. Genomics research revealed that dif- transformative ferent microbial species are adapted to discoveries detail- degrade specific types of hydrocarbon ing how microbes compounds (e.g., natural gases, ­straight-​ respond to petro- ­chain aliphatics, or aromatics) depending leum discharges on environmental conditions like tempera- and facilitate eco- ture and nutrient availability. These dis- system recovery. coveries underscore the natural capacity of Many of these microbes in the Gulf of Mexico and else- partnerships were where to bioremediate petroleum hydro- supported by the carbons. Gulf of Mexico Research Initiative How Oil Affects Ecosystems (GoMRI), created Scientists have long hypothesized that the with a $500 mil- fate and impacts of oil in ecosystems are lion, ­10-​­year com- determined by interplays between the mitment from BP physical and chemical characteristics of the to fund an inde- environment and by hydrocarbon chemistry pendent scientific and biogeochemical processes largely medi- research program ated by microbes. However, the complexity dedicated to of these interactions has impaired our abil- studying oil spill ity to decipher exactly how ecosystem func- impacts and miti- tioning is affected by oil. gation, particu- Oil can be a food source for some larly in the Gulf of microbes, but it can be toxic to others, Jonathan Delgardio and Will Overholt of the Georgia Institute of Technology sam- Mexico. GoMRI has resulting in adverse effects on microbially ple sand layers on 20 October 2010 at Pensacola Beach, Fla., which was heavily funded 17 interna- mediated ecosystem services like the break- polluted by weathered oil after Deepwater Horizon discharge. Researchers used tional consortia down of organic matter and the regenera- genomics to track how microbial communities changed in response to the oil by and thousands of tion of nutrients. Following the DWH comparing oiled sand layers to pristine sands. Credit: Markus Huettel investigators (bit​ discharge, GoMRI researchers observed .ly/GoM​­ -​ Research).­ through multiple lines of evidence that liq- Armed with genomics tools, Through a systems approach that incor- GoMRI researchers showed that ­oil-​ porates genomics along with knowledge and ­degrading microbes are, indeed, nearly tools from a range of other disciplines (e.g., ubiquitous, found almost everywhere In the wake of the biogeochemistry and oceanography), around the world in low abundance even researchers can now monitor and assess when crude oil is absent. These microbes, Deepwater Horizon spill, ecosystem health—and identify distur- part of the pool of low-abundance species bances that might otherwise go unnoticed— known as the rare biosphere, harbor a spe- multidisciplinary scientific by analyzing microbial populations that cialized metabolic capacity to use oil as a partnerships enabled both act as stewards for and represent bio- food source—a capability that can be rapidly indicators of ecosystems. With these activated upon exposure to oil [Kleindienst transformative discoveries efforts, global ecosystems can be better et al., 2015]. detailing how microbes protected and, when necessary, restored in From deep ocean waters to shallow the face of diverse environmental stressors. coastal sediments, ­hydrocarbon-​­degrading respond to petroleum bacteria responded profoundly to oil con- discharges and facilitate Transformative Discoveries tamination after the DWH spill, increasing Prior to 2010, most studies of microbes in abundance and expressing genes involved ecosystem recovery. associated with oil spills were conducted by in hydrocarbon metabolism over days to growing them in the laboratory using pure months. It was shown in some cases that cultures or enrichments. Consequently, we microbial communities were composed of uid and gaseous hydrocarbons from the spill had a very limited understanding of the up to 90% ­oil-​­degrading species after expo- rapidly entered the microbial food web and types and distribution of oil-­ ​­degrading sure to hydrocarbons [Kleindienst et al., 2015; persisted for years [­Fernández-​­Carrera et al., microorganisms—and of what they actually Huettel et al., 2018]. 2016; Rogers et al., 2019; Chanton et al., 2020], do—in the environment, because the vast Over time, successions of microbial pop- with major implications for carbon and majority of microorganisms in the natural ulations bloomed as they consumed the dif- nutrient cycling through the environment. environment have yet to be cultured. But in ferent hydrocarbon compounds of oil and ­Genomics-​­enabled research revealed, for the wake of the DWH spill, multidisciplinary responded to environmental factors [Kostka example, that ecosystem functions related

SCIENCE NEWS BY AGU // Eos.org 31 A sheen of oil coats the surface of the Gulf of Mexico in June 2010, as ships work to help control the Deepwater Horizon spill. Credit: kris krüg, CC BY-NC-SA 2.0 (bit.ly/ ccbyncsa2-0)

to the microbial nitrogen cycle were drasti- compounds disappeared. In addition, the dual capability to fix nitrogen and degrade cally affected by oil. abundances of genes related to degradation oil. Petroleum is made mostly of carbon and of specific hydrocarbon classes, such as contains relatively small amounts of major alkanes and polycyclic aromatics, could be “Superbug” Discovered nutrients like nitrogen and phosphorus. directly correlated with concentrations of Fertilizing water with nitrogen and phos- Thus, scientists expected that oiled envi- the corresponding classes. phorus to stimulate microbial growth is a ronments would likely become limited in Genomic data were corroborated by common bioremediation strategy for oil major nutrients, with negative effects research using isotopic tracers, which spill cleanup; it was used, for example, potentially rippling through entire food showed the incorporation of inorganic during the Valdez spill in 1989 [Bragg et al., webs. In numerous investigations of ­DWH-​ nitrogen into the microbial food web 1994]. But fertilizers are costly and difficult ­contaminated seawater and sediments, [­Fernández-​­Carrera et al., 2016]. ­Nitrogen-​ to apply over large scales and may result in genes for nitrogen fixation—a process car- ­fixing microbes, also called diazotrophs, unintended ecosystem consequences. ried out by some microbes that involves are well known to support crop growth in Thus, practitioners charged with cleaning converting inorganic nitrogen gas into fixed agricultural ecosystems and photosyn- up after oil spills dream of a “superbug”— forms like ammonium, which can be used thetic production in the open ocean [Zehr one that’s native to the contaminated by all organisms—were shown to increase et al., 2016], but nitrogen fixation by oil environment and capable of removing all many times relative to pristine conditions, degraders in response to hydrocarbon components of oil while also generating its even when adjusted for the overall abun- exposure is a new discovery. The recogni- own nutrients. dance of microbes present. tion that ­oil-​­degrading bacteria can supply Nature may have provided just such an For example, a metagenomic time series themselves with nitrogen indicates that organism. Guided by metagenomic field revealed an increase in the abundance of the microbial food web can compensate, at data, GoMRI researchers patched together genes that encode for nitrogen fixation (via least to an extent, for influxes of ­nutrient-​ the genomes of microbes thought to be the enzyme nitrogenase) that coincided ­poor oil. Studies by GoMRI researchers fur- diazotrophs that also degraded oil in marine with an increase in genes related to hydro- ther revealed that as overall microbial sediments. After looking at the potential carbon degradation pathways [­Rodriguez-​­R. diversity declined in oil-­ contaminated​­ metabolisms of these microbes, they iso- et al., 2015]. This increase then dissipated environments, the oil selected for a few lated a particular microorganism from the when the oil and associated hydrocarbon very abundant microbial species with the field samples. They used hexadecane, a

32 Eos // april 2020 hydrocarbon, as present in microbial communities, entific expertise, microbiologists can the sole carbon researchers can take the pulse of an ecosys- quickly and inexpensively analyze field and energy source tem and identify functional deficits or gains samples to provide essential information and did not pro- in the communities that affect the overall about microbial ecosystems before, during, vide any nitrogen health of the ecosystem. Such genomic and after spills. [Karthikeyan et al., indicators serve as biomarkers to guide mit- We envision a future in which omics 2019]. Sequencing igation strategies, much like blood tests can measurements enable assessment of envi- confirmed that the point physicians to disease diagnosis and ronmental risks, identification of ecosystem genome of the treatment options. deficits, selection of appropriate mitigation newly isolated During the DWH response, microbial plans, and monitoring of ecosystem recov- microbe, ­KTK-­01, genomics techniques have demonstrated the ery and in which scientists play key roles in contains genes potential to develop effective genetic proxies informing practitioners to improve that encode for or biomarkers for recording oil inputs, expo- response and restoration preparedness for nitrogen fixation sure regimes, and hydrocarbon degradation. future environmental disasters. and hydrocarbon ­Oil-​­induced ecosystem disruptions were degradation path- identified by a reduction in community References ways as well as for diversity; an overgrowth of certain species; Bragg, J. R., et al. 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(2016), Pulsed blooms and persistent oil-degrading in coastal environments around the world marine wells for oil and gas production and bacterial populations in the water column during and after the Deepwater Horizon blowout, Deep Sea Res., Part II, 129, 282–­ ​ and could prove to be a useful model because chemical dispersants—which may 291,­ https://doi​ .org/​ 10​­ .​ 1016/j­ .dsr2​ .2014​ .01​ .014.​ organism for further studying such be toxic to organisms—remain the major Zehr, J. P., et al. (2016), Unusual marine unicellular symbiosis with the nitrogen-­ fixing​­ cyanobacterium UCYN-­ A,​­ Nat. Microbiol., 2(1), responses. response strategy. But lessons learned from 16214, https://doi​ .org/​ 10​­ .​ 1038/­ nmicrobiol​­ .​ 2016­ .​ 214.­ DWH research so far can be applied to Oil Contamination Biomarkers developing new mitigation strategies and Author Information The ultimate goal of ­GoMRI-​­supported improvements in predictive capabilities for Joel E. Kostka (joel.​ kostka@biology­ .​ gatech­ ​ genomic research is to translate genomic responding to future environmental distur- .­edu), Georgia Institute of Technology, Atlanta; findings into actionable information to help bances, such as those caused by extreme Samantha Joye, University of Georgia, Athens; scientists monitor and restore ecosystem weather events or climate change. and Rita Colwell, University of Maryland, Col- health in the face of natural or ­human-​ For the first time, a ­data-​­driven approach lege Park ­made disasters. Through examination of the for oil spill response and mitigation is pos- organisms, genes, and metabolic pathways sible. With advanced genomic tools and sci- u Read the article at bit.ly/Eos­ -​ omics­

SCIENCE NEWS BY AGU // Eos.org 33