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Marine Bacterioplankton Community Turnover Within Seasonally Hypoxic Waters of a Subtropical Sound: Devil’S Hole, Bermuda

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Marine Bacterioplankton Community Turnover Within Seasonally Hypoxic Waters of a Subtropical Sound: Devil’S Hole, Bermuda bs_bs_banner Environmental Microbiology (2014) doi:10.1111/1462-2920.12445 Marine bacterioplankton community turnover within seasonally hypoxic waters of a subtropical sound: Devil’s Hole, Bermuda Rachel J. Parsons,1* Craig E. Nelson,2,3 community changes, including both direct counts and Craig A. Carlson,1,2 Carmen C. Denman,4,5 rRNA gene sequencing. During stratification, the Andreas J. Andersson,1,6 Andrew L. Kledzik,7 surface waters were dominated by the SAR11 clade of 4 1,8 Kevin L. Vergin, Sean P. McNally, Alphaproteobacteria and the cyanobacterium Syne- 4,9 4 Alexander H. Treusch and Stephen J. Giovannoni chococcus. In the suboxic bottom waters, cells 1Bermuda Institute for Ocean Science (BIOS), St. from the order Chlorobiales prevailed, with gene George’s, GE 01, Bermuda. sequences indicating members of the genera Chlo- 2Department of Ecology, Evolution and Marine Biology robium and Prosthecochloris – anoxygenic photo- and Marine Science Institute, University of California, autotrophs that utilize sulfide as a source of electrons Santa Barbara, CA, USA. for photosynthesis. Transitional zones of hypoxia also 3Center for Microbial Oceanography: Research and exhibited elevated levels of methane- and sulfur- Education, Department of Oceanography, University of oxidizing bacteria relative to the overlying waters. The Hawai‘i at Ma¯noa, Honolulu, HI, USA. abundance of both Thaumarcheota and Euryarcheota 4Department of Microbiology, Oregon State University, were elevated in the suboxic bottom waters (> 109 Corvallis, OR, USA. − cells l 1). Following convective mixing, the entire water 5London School of Hygiene and Tropical Medicine, column returned to a community typical of oxygen- London, UK. ated waters, with Euryarcheota only averaging 5% of 6Scripps Institution of Oceanography, University of cells, and Chlorobiales and Thaumarcheota absent. California San Diego, San Diego, CA, USA. 7Department of Marine and Environmental Systems, Introduction Florida Institute of Technology, Melbourne, FL, USA. 8College of the Environment and Life Sciences, The The importance of planktonic Bacteria and Archaea University of Rhode Island, Kingston, RI, USA. (referred to henceforth as bacterioplankton; Pace, 2006) 9Department of Biology, Nordic Centre for Earth and their role in ocean biogeochemical cycles are Evolution, University of Southern Denmark, Odense, well established; they are involved in virtually all the Denmark. biogeochemical reactions occurring in the oceans (Kirchman, 2008). High primary productivity in stratified Summary shallow coastal waters can lead to the seasonal develop- ment of suboxic and anoxic bottom waters. The develop- Understanding bacterioplankton community dyna- ment of these oxygen minimum zones is increasing in mics in coastal hypoxic environments is relevant strength, duration and extent because of the combined to global biogeochemistry because coastal hypoxia effects of eutrophication and climate change (Diaz and is increasing worldwide. The temporal dynamics Rosenberg, 2008; Stramma et al., 2010; Howarth et al., of bacterioplankton communities were analysed 2011; Wright et al., 2012). Physical mixing serves to ven- throughout the illuminated water column of Devil’s tilate portions of the water column and, if sufficiently deep, Hole, Bermuda during the 6-week annual transition can entrain nutrient rich deep water to the surface, eradi- from a strongly stratified water column with suboxic cating both oxygen minimum zones and redox gradients. and high-pCO2 bottom waters to a fully mixed and For example, the hurricanes in the Gulf of Mexico are ventilated state during 2008. A suite of culture- often strong enough to disrupt hypoxia on the Louisiana independent methods provided a quantitative spat- shelf (Rabalais et al., 2009). Alternating seasonal patterns iotemporal characterization of bacterioplankton of mixing followed by restratification can consequently regulate nutrient fluxes (Zehr and Ward, 2002) and create Received 6 November, 2013; accepted 23 February, 2014. *For cor- respondence. E-mail [email protected]; Tel. 1 441 297 1880 ecosystem shifts in bacterioplankton community structure x726; Fax 1 44 297 8143. (Giovannoni and Vergin, 2012). © 2014 Society for Applied Microbiology and John Wiley & Sons Ltd 2 R. J. Parsons et al. Hypoxic environments are characterized by the deple- Despite the fact that microbial processes dominate in tion of oxygen with some demonstrating elevated con- anoxic and suboxic ecosystems, temporal patterns of centrations of sulfides (Stewart et al., 2007). Sulfide bacterial succession have been studied in only a handful production can result from sulfate reduction coupled of systems (Stal et al., 1985; Crump et al., 2007; Zaikova to the oxidation of reduced carbon compounds such as et al., 2010). Bacterial community succession has been methane (Stewart et al., 2007) or through the oxidation of associated with substrate concentrations in soils (Noll organic matter where sulfate is used as the electron et al., 2004), oxygen availability in estuaries (Crump et al., acceptor rather than oxygen (Fenchel et al., 2012). 2007), oxygen and phosphate gradients in fjords (Zaikova Oxygen is the most thermodynamically favoured terminal et al., 2010), and nitrogen fixation and light availability in electron acceptor followed by nitrate, nitrite then sulfate cyanobacteria mats within sandy sediments (Stal et al., and finally carbon dioxide (Wright et al., 2012). This 1985). sequence is used to define specific microbial niches that Devil’s Hole, Bermuda (32°19.399′ N, 64°43.08′ W) span oxygen ranges divided into oxic (> 90 μmol l−1); was used as a natural laboratory to examine the succes- dysoxic (20–90 μmol l−1); suboxic (1–20 μmol l−1) and sion of the bacterioplankton community structure as anoxic (< 1 μmol l−1) conditions (Wright et al., 2012). dysoxia and suboxia developed and subsequent turnover The removal of oxygen, increase in pCO2 and subse- occurred. The study site was within the euphotic zone and quent decrease in pH all can play important roles in con- experiences seasonal thermal stratification resulting in trolling bacterioplankton community structure and function hypoxia below the base of the subthermocline layer. within this redoxcline (Brune et al., 2000; Taylor et al., Devil’s Hole is located in the shallow coastal embayment 2001). Adaptations to fluctuations in oxygen conditions, of Harrington Sound, Bermuda. Harrington Sound is specifically at the oxycline, in combination with elevated approximately 5 km2 with a mean bottom depth of 14.5 m H2S and ammonium concentrations can enable spe- (Fig. 1). Devil’s Hole is the deepest part of the sound, a cialized bacterioplankton populations, such as H2S and former sinkhole with a bottom depth of ∼25 ± 1 m below ammonium-oxidizing bacterioplankton to colonize micro- the surface (depending on tidal height). Harrington Sound niches (Brune et al., 2000) and contribute to organic is linked to Bermuda’s North Shore reef platform via a matter production via chemoautotrophy (Taylor et al., narrow inlet (Flatts Inlet, < 20 m wide) providing the main 2001; Francis et al., 2007). In systems where the source of surface water tidal exchange (along with addi- redoxcline occurs in the euphotic zone (e.g. the Black tional subterranean water exchange). The nominal resi- Sea), organisms such as anaerobic photolithoautotrophic dence time of water in the sound is approximately 30 days green sulfur bacteria populate the oxycline (Repeta et al., with respect to the semidiurnal tidal flow, but effective tidal 1989). For example, Chlorobium sp. are low light-adapted mixing can be as long as 4 months (Brown, 1978; 1980). photolithotrophic oxidizers of H2S that are capable of The physical and chemical properties of Harrington fixing CO2 to organic matter under suboxic or anoxic water Sound (and Devil’s Hole) have been studied extensively conditions (Kim and Chang, 1991; Overmann et al., 1992; for over 40 years (Thorstenson and Mackenzie, 1974; Taipale et al., 2009). Morris et al., 1977; Andersson et al., 2007). Fig. 1. Inset – Map of Bermuda. Outset – Harrington Sound Map showing depth in contours (every 10 ft or 3 m) with Devil’s Hole located in the Southeast corner with the deepest depth (80 ft or 24.4 m). The only exchange with offshore water is through Flatts Inlet. The map is adopted from (Andersson et al., 2007). © 2014 Society for Applied Microbiology and John Wiley & Sons Ltd, Environmental Microbiology Bacterioplankton turnover within seasonally hypoxic waters 3 This study consisted of a short time series in which 2004). TRFLP, FISH and flow cytometry data were used water column biogeochemistry and bacterioplankton com- to select a subset of samples for deeper community in- munity structure were monitored at Devil’s Hole from terrogation using both Sanger sequencing and 454 August to November 2008, a period during which hypoxia pyrosequencing of 16S rRNA gene amplicons. By com- formed under stratified conditions (August–September) bining these approaches with a comprehensive suite of and was eroded under convective mixing conditions microbial, hydrographic and biogeochemical measure- (October–November), a cycle that occurs annually. We ments (including temperature, salinity, pCO2,O2, viral employed multiple complementary culture-independent and bacterial densities, and inorganic nitrogen and phos- methods to characterize the succession- and mixing- phorous concentrations), we are able to present a cohe- induced change of the bacterioplankton communities
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