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Diverse, Rare Microbial Taxa Responded to the Deepwater Horizon Deep-Sea Hydrocarbon Plume

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Diverse, Rare Microbial Taxa Responded to the Deepwater Horizon Deep-Sea Hydrocarbon Plume The ISME Journal (2016) 10, 400–415 © 2016 International Society for Microbial Ecology All rights reserved 1751-7362/16 OPEN www.nature.com/ismej ORIGINAL ARTICLE Diverse, rare microbial taxa responded to the Deepwater Horizon deep-sea hydrocarbon plume Sara Kleindienst1,4, Sharon Grim2,5, Mitchell Sogin2, Annalisa Bracco3, Melitza Crespo-Medina1,6 and Samantha B Joye1 1Department of Marine Sciences, University of Georgia, Athens, GA, USA; 2Josephine Bay Paul Center, Marine Biological Laboratory, Woods Hole, MA, USA and 3School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA, USA The Deepwater Horizon (DWH) oil well blowout generated an enormous plume of dispersed hydrocarbons that substantially altered the Gulf of Mexico’s deep-sea microbial community. A significant enrichment of distinct microbial populations was observed, yet, little is known about the abundance and richness of specific microbial ecotypes involved in gas, oil and dispersant biodegradation in the wake of oil spills. Here, we document a previously unrecognized diversity of closely related taxa affiliating with Cycloclasticus, Colwellia and Oceanospirillaceae and describe their spatio-temporal distribution in the Gulf’s deepwater, in close proximity to the discharge site and at increasing distance from it, before, during and after the discharge. A highly sensitive, computational method (oligotyping) applied to a data set generated from 454-tag pyrosequencing of bacterial 16S ribosomal RNA gene V4–V6 regions, enabled the detection of population dynamics at the sub-operational taxonomic unit level (0.2% sequence similarity). The biogeochemical signature of the deep-sea samples was assessed via total cell counts, concentrations of short-chain alkanes (C1–C5), nutrients, (colored) dissolved organic and inorganic carbon, as well as methane oxidation rates. Statistical analysis elucidated environmental factors that shaped ecologically relevant dynamics of oligotypes, which likely represent distinct ecotypes. Major hydrocarbon degraders, adapted to the slow-diffusive natural hydrocarbon seepage in the Gulf of Mexico, appeared unable to cope with the conditions encountered during the DWH spill or were outcompeted. In contrast, diverse, rare taxa increased rapidly in abundance, underscoring the importance of specialized sub- populations and potential ecotypes during massive deep-sea oil discharges and perhaps other large-scale perturbations. The ISME Journal (2016) 10, 400–415; doi:10.1038/ismej.2015.121; published online 31 July 2015 Introduction from the broken riser pipe, altering deepwater chemistry in the vicinity of the Macondo wellhead. The largest open ocean hydrocarbon discharge in The jet of oil and gas ascending into the water column history released unprecedented quantities of gas and entrained cold seawater (Johansen et al., 2001; oil into the deep ocean of the Northern Gulf of Socolofsky et al., 2011) and generated a prolific Mexico (hereafter referred to as the Gulf) following hydrocarbon-rich deepwater plume that was detected the explosion and sinking of the Deepwater Horizon to the southwest of the well by its fluorescence (DWH) offshore drilling platform in 2010. Early signature (Camilli et al., 2010; Diercks et al., 2010; during the DWH incident, before the damaged riser Hazen et al., 2010), and light scattering profile pipe was cut, hydrocarbon injection into the water (Diercks et al., 2010), as well as by elevated column occurred as a pronounced jet that emerged concentrations of specific hydrocarbons (Camilli et al., 2010; Diercks et al., 2010; Valentine et al., Correspondence: S Joye, Department of Marine Sciences Uni- 2010; Joye et al., 2011; Kessler et al., 2011b; Reddy versity of Georgia, Room 220 Marine Sciences Building, Athens, et al., 2012) and of the dispersant Corexit (Kujawinski GA, 30602-3636, USA. et al., 2011). The deepwater plume spanned depths E-mail: [email protected] between 1000 and 1300 m, in a region at least 35 km 4Present address: Center for Applied Geosciences, Eberhard-Karls- University Tuebingen, 72074 Tuebingen, Germany. long by 2 km wide (Camilli et al., 2010). 5Present address: Department of Earth and Environmental Early in the DWH discharge, the hydrocarbon- Sciences, University of Michigan, Ann Arbor, MI, USA. impacted deep-sea waters hosted significantly 6Present address: Center for Environmental Education, Conserva- enriched bacterial populations related to Oceanos- tion and Research, Inter American University of Puerto Rico, San Juan, Puerto Rico. pirillum, Cycloclasticus, Colwellia, Pseudoalteromonas, Received 31 October 2014; revised 21 May 2015; accepted Rhodobacterales and methylotrophs (Mason et al., 2012; 3 June 2015; published online 31 July 2015 Reddy et al., 2012; Redmond and Valentine, 2012; Microbial response to the DWH hydrocarbon plume S Kleindienst et al 401 Valentine et al., 2012). In situ observations and would converge into a single OTU (Eren et al., laboratory findings signal that these bacteria played 2013). The ecologically powerful index of Shannon key roles in the biodegradation of oil in the plume. entropy ignores stochastic variation, for example, Compositional changes in hydrocarbon abundance sequencing error, and uses information-rich sites to implied preferential microbial utilization of disaggregate similar sequences into oligotypes that oil-derived short-chain and higher-molecular weight represent discrete microbial populations in commu- alkanes (Valentine et al., 2010; Kessler et al., 2011b), nities sampled from different ecological contexts. whereas local dissolved oxygen anomalies Dissimilarity thresholds for oligotypes can be as low (Joye et al., 2011; Kessler et al., 2011a, b) indicated as 0.2%, versus the commonly used 3% obtained extensive aerobic alkane respiration (Valentine et al., using OTU clustering. 2010; Crespo-Medina et al., 2014). Furthermore, In this work, we delved into the microbial stable-isotope probing and single-cell genomics diversity of the DWH deepwater hydrocarbon plume identified microbial populations involved in hydro- to an extent not attempted previously. We report an carbon degradation or enrichment of metabolic genes unrecognized level of diversity among key micro- that orchestrate hydrocarbon degradation in the organisms involved in hydrocarbon degradation, and plume, with Colwellia likely oxidizing ethane and describe their spatio-temporal response to the oil, gas propane (Redmond and Valentine, 2012), Oceanos- and dispersant infusion into the Gulf’s deepwaters. pirillum degrading cyclohexane (Mason et al., 2012) Samples were obtained before, during and after the and Cycloclasticus utilizing polycyclic aromatic discharge, in close proximity to the discharge site hydrocarbons (PAH) (Yakimov et al., 1998). and at increasing distance from it (Table 1). We Descriptions of microbial communities using large surveyed microbial population dynamics of closely marker gene data sets in combination with well- related taxa through oligotype analysis of bacterial characterized environmental parameters offer a 16S rRNA genes. The geochemical signature of the powerful method to evaluate the dynamic responses plume fluids characterized the environmental factors of bacterial assemblages to altered ecological condi- that drove the observed remarkable shifts in relative tions. The common approach of 16S ribosomal RNA abundance for closely related microbial taxa, which (rRNA) gene sequence taxon assignments typically likely represent distinct ecotypes. relies on sequence similarity thresholds (for example, 97%) to identify operational taxonomic units (OTUs), aiming to minimize the influence of random sequen- Materials and methods cing errors (Huse et al., 2010; Kunin et al., 2010). Although distribution patterns of OTUs among Study sites environmental samples are frequently used to infer Samples were obtained from the northern Gulf of ecological functions of microbial populations, this Mexico (Table 1,Supplementary Figure S1), on approach does not detect small variations in the 16S cruises R/V Pelican (PE 10-20, March 2010), R/V rRNA gene sequence that reflects different ecotypes Walton Smith (WS1010, May/June 2010), R/V Ocea- (Ward, 1998; Eren et al., 2013). The ecotype concept nus (OC468-2, September 2010), R/V Atlantis describes a collection of strains with subtly different (AT18-2, November 2010), R/V Endeavor (EN496, genetic elements, which afford the ability to occupy July 2011), R/V Endeavor (EN510, June 2012) and slightly different ecological niches while preserving R/V Falkor (FA006, November 2012). The DWH the genetic signature and the (nearly) full ecophysio- wellhead is located in Mississippi Canyon block 252 logical potential (Konstantinidis and Tiedje, 2005). (latitude 28.7381, longitude -88.3659; hereafter Ecological distinctiveness of closely related popula- MC252). Samples impacted by the DWH discharge tions could for instance be indicated by growth on a were taken within the plume (water depth from 1000 new substrate or by metabolic plasticity, for example, to 1300 m), above the plume or below the plume. In carrying out multiple metabolisms depending on addition, we sampled different locations over an area environmental conditions (Konstantinidis et al., of approximately 105 000 km2 to assess the impact of 2006). Such metabolic flexibility was almost certainly the deepwater plume. For ease of sample identifica- advantageous for diverse taxa present in the wake of tion, samples were numbered (1–20) and designated the
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