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Bacteriochlorophyll and Community Structure of Aerobic Anoxygenic Phototrophic Bacteria in a Particle-Rich Estuary

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Bacteriochlorophyll and Community Structure of Aerobic Anoxygenic Phototrophic Bacteria in a Particle-Rich Estuary The ISME Journal (2010) 4, 945–954 & 2010 International Society for Microbial Ecology All rights reserved 1751-7362/10 $32.00 www.nature.com/ismej ORIGINAL ARTICLE Bacteriochlorophyll and community structure of aerobic anoxygenic phototrophic bacteria in a particle-rich estuary Matthew T Cottrell1, Josephine Ras2 and David L Kirchman1 1University of Delaware, School of Marine Science and Policy, Lewes, DE, USA and 2Laboratoire d’Oce´anographie de Villefranche-sur-mer, UMR 7093 CNRS et Universite´ Pierre et Marie Curie, Villefranche-sur-Mer Cedex, France Photoheterotrophic microbes use organic substrates and light energy to satisfy their demand for carbon and energy and seem to be well adapted to eutrophic estuarine and oligotrophic oceanic environments. One type of photoheterotroph, aerobic anoxygenic phototrophic (AAP) bacteria, is especially abundant in particle-rich, turbid estuaries. To explore questions regarding the controls of these photoheterotrophic bacteria, we examined their abundance by epifluorescence microscopy, concentrations of the light-harvesting pigment, bacteriochlorophyll a (BChl a) and the diversity of pufM and 16S ribosomal RNA (rRNA) genes in the Chesapeake Bay. Concentrations of BChl a varied substantially, much more so than AAP bacterial abundance, along the estuarine salinity gradient. The BChl a concentration was correlated with turbidity only when oceanic and estuarine waters were considered together. Concentrations of BChl a and BChl a quotas were higher in particle-associated than in free-living AAP bacterial communities and appear to reflect physiological adaptation, not different AAP bacterial communities; pufM genes did not differ between particle-associated and free- living communities. In contrast, particle-associated and free-living bacterial communities were significantly different, on the basis of the analysis of 16S rRNA genes. The BChl a quota of AAP bacteria was not correlated with turbidity, suggesting that pigment synthesis varies in direct response to particles, not light attenuation. The AAP bacteria seem to synthesize more BChl a when dissolved and particulate substrates are available than when only dissolved materials are accessible, which has implications for understanding the impact of substrates on the level of photoheterotrophy compared with heterotrophy in AAP bacteria. The ISME Journal (2010) 4, 945–954; doi:10.1038/ismej.2010.13; published online 25 February 2010 Subject Category: microbial ecology and functional diversity of natural habitats Keywords: AAP bacteria; bacteriochlorophyll; Chesapeake Bay; photoheterotrophy Introduction et al., 2004; Michelou et al., 2007; Mary et al., 2008). Nonetheless, there are large gaps in our under- Photoheterotrophic microbes satisfy their require- standing of how photoheterotrophic microbes adapt ment for carbon and energy by consuming organic to light, dissolved organic carbon, particulate substrates and harvesting light energy. Photohetero- organic carbon and nutrients. Estuaries present trophy is widespread among the main groups of valuable test cases for examining the relationship microbes found in aquatic systems, including between photoheterotrophs and these environmental cyanobacteria, Proteobacteria and Bacteroidetes factors. (Eiler, 2006) and is integral to microbial carbon One group of photoheterotrophs, the aerobic and energy cycling in estuarine, coastal and oceanic anoxygenic phototrophic (AAP) bacteria, seems to waters. Measurements of light-stimulated bacterial be more abundant in estuarine waters than in other production and amino-acid assimilation suggest that environments. The highest abundances of AAP photoheterotrophy contributes directly to the flux of bacteria occur in estuaries, such as Long Island carbon (C) and energy in marine systems (Church Sound, Chesapeake Bay and Delaware Bay, where these bacteria can constitute more than 10% of total prokaryotic abundance (Schwalbach and Fuhrman, Correspondence: DL Kirchman, School of Marine Science and 2005; Waidner and Kirchman, 2007). Although Policy, University of Delaware, 700 Pilottown Rd, Lewes, DE ranging up to almost 25% of the total prokaryotic 19958, USA. E-mail: [email protected] community in the oligotrophic South Pacific Ocean Received 4 November 2009; revised 19 January 2010; accepted 20 (Lami et al., 2007), AAP bacterial abundance is January 2010; published online 25 February 2010 typically less than 10% of the total community in BChl and community structure of AAP bacteria MT Cottrell et al 946 oceanic environments. The AAP bacteria make up ecology of AAP bacteria. Particle-associated and 1.5–15% of total prokaryotic abundance in the free-living cells were examined to determine the coastal Pacific Ocean off California (Schwalbach relationship between these photoheterotrophs and and Fuhrman, 2005), in tropical and polar waters concentrations of particulate detritus. Phylogenetic (Schwalbach and Fuhrman, 2005; Cottrell and analyses of free-living and particle-associated Kirchman, 2009), in the North Atlantic Ocean AAP bacteria were used to explore the impact of (Sieracki et al., 2006) and in shelf waters of the physiological adaptation versus shifts in community mid-Atlantic bight and in the Pacific Ocean near structure on the BChl a quota of AAP bacteria. Hawaii (Cottrell et al., 2006). Abundances of AAP bacteria in the brackish Baltic Sea, which is much like an estuary with a large input of freshwater Materials and methods (Stepanauskas et al., 2002), seem to be more similar Sampling and oceanographic parameters to those found in the ocean, ranging from about The main stem of Chesapeake Bay was sampled 1–10% of the total prokaryotes (Salka et al., 2008). in June 2006. Seawater was collected from a depth Bacteriochlorophyll a (BChl a) is the light-harvest- of approximately 1 m using Niskin bottles (General ing pigment and a component of the reaction center Oceanics, Miami, FL, USA). Light attenuation was complex in AAP bacteria (Yurkov and Beatty, 1998; measured using a Secchi disc (Wildlife Supply Kolber et al., 2001). The concentration of BChl a in B Company, Yulee, FL, USA) and a Biospherical oligotrophic waters is low ( 1%) compared with (San Diego, CA, USA) light meter. Salinity was that of chlorophyll a (Goericke, 2002; Cottrell et al., determined using an SBE-9 conductivity meter 2006; Sieracki et al., 2006; Lami et al., 2007). Never- (Sea-Bird Electronics, Bellevue, WA, USA). Free- theless, the BChl a quota of AAP bacteria cells can living microbes were separated from the whole be substantial and comparable to the divinyl- community by size-fractionation using vacuum filtra- chlorophyll a quota of Prochlorococcus (Cottrell tion and 0.8-mm pore-size polycarbonate (Millipore, et al., 2006). Such an investment by AAP bacteria Billerica, MA, USA) filters. Chlorophyll a (Chl a)was in BChl a synthesis suggests that light harvesting is measured by fluorometry using 90% acetone extracts an important aspect of AAP bacterial metabolism. of particulate material collected on GF/F (Whatman, The BChl a quota of cultivated AAP bacteria varies Piscataway, NJ, USA) filters (Parsons et al., 1984). as much as 10-fold in response to light availability (Koblı´zek et al., 2003; Li et al., 2006), similar to Synechococcus and Prochlorococcus (Mackey et al., Microscopic enumeration of AAP bacteria and total 2009). In addition, the BChl a quota of AAP bacteria prokaryotes is higher at night than during the day because Prokaryotes were enumerated by epifluorescence BChl a synthesis is inhibited by light (Koblı´zek microscopy of paraformaldehyde-fixed samples that et al., 2005, 2007). However, in oceanic waters the were filtered onto 0.2-mm pore-size black polycarbo- BChl a quota of AAP bacteria does not seem to vary nate filters. Total prokaryotes were enumerated after systematically with depth in the water column staining with a solution of 1 mgmlÀ1 40,6-diamidino- (Cottrell et al., 2006), suggesting that factors other 2-phenylindole (Porter and Feig, 1980) in Tris buffer than light alone may impact the pigment quota of (pH 7.2) containing 0.5 M NaCl. The samples were AAP bacteria. analyzed using a computer-controlled microscope Particle attachment seems to be a key adaptation (Olympus Provis AX70, Central Valley, PA, USA) for the success of AAP bacteria. In Delaware Bay, and image analysis software (ImagePro Plus, Media 30–90% of AAP bacteria are associated with Cybernetics, Bethesda, MD, USA) as described particles, whereas usually 20% or less of total previously (Cottrell and Kirchman, 2003). The prokaryotes are particle associated (Waidner and average and s.d. value for 20 fields of view were Kirchman, 2007). However, high percentages of estimated. The AAP bacteria were enumerated using particle-associated AAP bacteria may be specific to an Intensified Retiga charge-couple device camera estuaries. In the Atlantic Ocean and Mediterranean (Qimaging, Surry, BC Canada) and image analysis Sea, 10–40% of AAP bacteria appeared to be routines to enumerate cells that fluoresce blue when associated with particles, whereas in a Mediterra- stained with 40,6-diamidino-2-phenylindole and nean coastal lagoon about 50% of AAP bacteria were have infra-red fluorescence, but not red or orange associated with particles (Lami et al., 2009). Adap- fluorescence (Cottrell et al., 2008; Cottrell and tations to the particle environment may involve Kirchman, 2009). responses to the availability of light controlled, in part, by light scattering and absorption by particles and to the availability
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