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Characterization of Purple Sulfur Bacteria from the South Andros

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Characterization of Purple Sulfur Bacteria from the South Andros Blackwell Science, LtdOxford, UKEMIEnvironmental Microbiology 1462-2912Society for Applied Microbiology and Blackwell Publishing Ltd, 2005Original ArticlePhototrophic bacteria in the South Andros Black HoleR. A. Herbert et al. Environmental Microbiology (2005) doi:10.1111/j.1462-2920.2005.00815.x Characterization of purple sulfur bacteria from the South Andros Black Hole cave system: highlights taxonomic problems for ecological studies among the genera Allochromatium and Thiocapsa Rodney A. Herbert,1* Anthony Ranchou-Peyruse,2 lems within these genera. These inconsistencies may Robert Duran,2 Rémy Guyoneaud2 and have implications for microbiologists studying the Stephanie Schwabe3 ecology of anoxygenic phototrophs. For ecologists 1Division of Environmental and Applied Biology, Biological studying the functioning of an ecosystem it may not Sciences Institute, University of Dundee, Dundee DD1 be particularily important to know whether a specific 4HN, Scotland. isolate belongs to one species or another. However, 2Laboratoire d’Ecologie Moléculaire-Microbiologie, if one wants to study the role of different populations EA3525, IBEAS, Université de Pau, BP1155, 64013 Pau, within a particular functional group then the species France. concept is important. This study demonstrates that 3Rob Palmer Blue Holes Foundation, 5 Longtitude Lane, further work is still required on the taxonomy of Charleston, SC 29401, USA. purple sulfur bacteria in order that microbial ecolo- gists are able to accurately identify a population/ species isolated from hitherto undescribed aquatic Summary ecosystems. A dense 1 m thick layer of phototrophic purple sulfur bacteria is present at the pycnocline (17.8 m depth) in Introduction the meromictic South Andros Black Hole cave system (Bahamas). Two purple sulfur bacteria present in sam- Phototrophic purple sulfur bacteria are widely distributed ples collected from this layer have been identified as in nature where oxygen is either absent or present at low belonging to the family Chromatiaceae. One isolate concentrations and opposing, yet overlapping, gradients (BH-1), pink coloured, is non-motile, non-gas vacu- of sulfide and light are simultaneously present. The larg- olated, 2–3 mm in diameter and surrounded by a cap- est and most significant developments of phototrophic sule. The other isolates (BH-2 and BH-2.4), reddish- sulfur bacteria occur in lacustrine environments (Taka- brown coloured, are small celled (4 mm ¥ 2 mm), motile hashi and Ichimura, 1968; Caldwell and Tiedje, 1975; by means of a single polar flagellum. In both isolates Guerrero et al., 1987; Pfennig and Trüper, 1989; Over- (BH-1 and BH-2), the intracellular photosynthetic mann et al., 1991; 1996). In stratified lakes phototrophic membranes are of the vesicular type and bacterio- sulfur bacteria often form dense blooms during the sum- chlorophyll a and carotenoids of the normal spirillox- mer months just below the chemocline and can contribute anthin series are present. Both isolates grow well in significantly to the primary production of these bodies of the presence of sulfide and carbon dioxide in the water (Wetzel, 1973; Biebl and Pfennig, 1979; Overmann light. During photoautotrophic growth sulfur globules et al., 1996). Sulfide required by the phototrophic bacteria are stored intracellularily as intermediate oxidation as electron donor during anoxygenic photosynthesis is products. According to the 16S rRNA gene sequence generated as an end-product of dissimilatory sulfate data the isolates belong to the genera Thiocapsa and reduction by sulfate-reducing bacteria, which are depen- Allochromatium. However, at the species level a num- dent on a supply of organic matter as a source of energy ber of inconsistencies exist between the phenotypic and carbon. In contrast to the marine environment, micro- and phylogenetic data, highlighting taxonomic prob- bial sulfate reduction in freshwater habitats is often limited by sulfate availability. However, where lakes develop in porous sedimentary rocks such as limestone or in close proximity to the sea, high levels of sulfate are commonly Received 26 October 2004; accepted 22 February 2005. *For corre- found either arising from gypsum dissolution or by seep- spondence. E-mail [email protected]; Tel. (+44) 1382 3462; Fax (+44) 1382 3442 75. This paper is dedicated to Professor Norbert age of seawater through fissures and fractures in the rock Pfennig on the occasion of his 80th birthday. (Guerrero et al., 1987; Matsuyama, 1987). © 2005 Society for Applied Microbiology and Blackwell Publishing Ltd 2 R. A. Herbert et al. The rock platform on which the islands of the Bahamas surrounded by a capsule. Bright-field microscopy showed sit is composed almost entirely of limestone (Sealey, the presence of sulfur globules within the cells but gas 1994). Within the porous carbonate platform of these low vesicles were absent irrespective of the growth conditions lying islands some of the world’s most spectacular cave tested (light and temperature). Examination of ultrathin systems have developed (Palmer, 1985). The most spec- sections by electron microscopy showed the presence of tacular of these, with respect to scale, is the South Andros an internal membrane system of the vesicular type. In Black Hole. The almost circular entrance to this water- contrast, cells of isolate BH-2 were motile with individual filled vertical cave system has a diameter of 300 ± 15 m cells 3–4 mm long and between 1.8 and 2.5 mm in width. and a depth of 47 m (Schwabe and Herbert, 2004). The The cells were straight rods and electron microscopy of water column comprises an upper brackish water mass uranyl-acetate-stained cells showed the presence of a (12‰ salinity) overlying a denser saline layer (35‰ salin- single polar flagellum. Older cultures showed a tendency ity). At the pycnocline (17.8 m) a 1 m thick layer of pho- to lose their motility and form dense clumps at the bottom totrophic purple sulfur bacteria was present. Coincident of the vials. Electron microscopy of ultrathin sections with the microbial layer the water temperature increased revealed the presence of an internal membrane system sharply from 29∞C to 36∞C before returning to 29∞C at of the vesicular type. There was no evidence to indicate, 20 m depth. Similarly, the dissolved oxygen concentration either from ultrastructure studies or incubation at low light which had an almost constant value of 6 mg l-1 in the intensities and/or low temperatures that isolate BH-2 pro- upper brackish water mass decreased sharply at the pyc- duced gas vesicles. nocline to < 1 mg l-1 while the pH decreased from pH 8.6 to pH 6.45. Sulfide which was absent from the upper water Photosynthetic pigments mass was present at a concentration of 30 mM in the phototrophic layer. Dense populations of photoautotrophically grown cultures This present study describes the morphological and of isolate BH-1 were pale pink when the cells were full of physiological characteristics of two purple sulfur bacte- elemental sulfur and became a progressively darker pink ria present in the microbial layer. Their taxonomic posi- when they became sulfur depleted. The in vivo absorption tion is discussed according to the current classification spectrum of sulfur-depleted cells exhibited the typical of anoxygenic phototrophs belonging to the family absorption spectrum of bacteriochlorophyll a with maxima Chromatiaceae. at 375, 590, 802 and 858 nm. Absorption maxima at 488, 515 and 550 nm were indicative of the presence of caro- tenoids of the normal spirilloxanthin series (Pfennig and Results Trüper, 1992) with spirilloxanthin as the dominant caro- From water samples collected from the 1 m thick microbial tenoid (Schmidt et al., 1965). Quantitative high-perfor- layer at a depth of 18 m in the South Andros Black Hole mance liquid chromatography (HPLC) chromatography enrichment cultures for phototrophic bacteria were set up. confirmed that spirilloxanthin accounted for 91% of the The enrichment cultures were incubated in the light and carotenoids together with a novel carotenoid tentatively samples periodically removed aseptically for identified as spirilloxanthin-2-ol (8%). Mass cultures of microscopical examination. After 2–3 weeks of incubation isolate BH-2 were pinkish-red when full of elemental sulfur the enrichment cultures began to appear pinkish red and becoming a darker red when depleted. In vivo absorption phase-contrast microscopy showed the presence of non- of cell suspensions is typical of bacteriochlorophyll a con- motile spherical cells and motile rod-shaped cells, both of taining phototrophs (ë maxima 375, 592, 800 and which accumulated elemental sulfur intracellularily. After 853 nm). As observed for isolate BH-1, the absorption repeated passage through deep agar dilution series pure maxima of 488, 515 and 550 nm indicate the presence of cultures of purple sulfur bacteria were obtained from the carotenoids of the normal spirilloxanthin series. Quantita- highest dilutions. Isolate BH-1 had morphological charac- tive HPLC chromatography revealed rhodopin as major teristics similar to members of the genus Thiocapsa. Iso- carotenoid (65%) and a substantial amount of spirilloxan- lates BH-2 and BH-2.4 had a morphology resembling that thin (25%) relative to lycopene (3%). of small-celled, motile member of the Chromatiaceae. Only strains BH-1 and BH-2 were further studied for phe- Physiological characteristics notypic characterization. When grown under anoxic conditions in the light isolate BH-1 grew well photoautotrophically
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