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First Description of a New Uncultured Purple Sulfur Bacterium Colonizing Marine Mangrove Sediment in the Caribbean

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First Description of a New Uncultured Purple Sulfur Bacterium Colonizing Marine Mangrove Sediment in the Caribbean First description of a new uncultured purple sulfur bacterium colonizing marine mangrove sediment in the Caribbean: Halochromatium-like PSB from Guadeloupe Olivier Gros, Laurie Bisqué, Mélissa Sadjan, Catherine Azede, Patrick Jean-Louis, Chantal Guidi-Rontani To cite this version: Olivier Gros, Laurie Bisqué, Mélissa Sadjan, Catherine Azede, Patrick Jean-Louis, et al.. First de- scription of a new uncultured purple sulfur bacterium colonizing marine mangrove sediment in the Caribbean: Halochromatium-like PSB from Guadeloupe. Comptes Rendus Biologies, Elsevier Masson, 2018, 341 (7-8), pp.387 - 397. 10.1016/j.crvi.2018.07.001. hal-01884590 HAL Id: hal-01884590 https://hal.sorbonne-universite.fr/hal-01884590 Submitted on 1 Oct 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License C. R. Biologies 341 (2018) 387–397 Contents lists available at ScienceDirect Comptes Rendus Biologies ww w.sciencedirect.com Microbiology: bacteriology, mycology, parasitology, virology / Microbiologie : bacte´riologie, mycologie, parasitologie, virologie First description of a new uncultured purple sulfur bacterium colonizing marine mangrove sediment in the Caribbean: Halochromatium-like PSB from Guadeloupe Description d’une bacte´rie sulfureuse pourpre non cultivable colonisant les se´diments des mangroves marine dans la Caraı¨be : Halochromatium- like PSB de Guadeloupe a,b, a a a Olivier Gros *, Laurie Bisque´ , Me´lissa Sadjan , Catherine Azede , a a Patrick Jean-Louis , Chantal Guidi-Rontani a Sorbonne Universite´s,UPMCUniversite´ Paris-6, Universite´ des Antilles,CNRS, E´volution Paris Seine–Institut de biologie Paris Seine (EPS–IBPS), 75005 Paris, France b C3MAG, UFR des sciences exactes et naturelles, Universite´ des Antilles, BP 592, 97159 Pointe-a`-Pitre, Guadeloupe A R T I C L E I N F O A B S T R A C T Article history: Here, we report the first description of a marine purple sulfur bacterium (PSB) from sulfide-rich Received 27 December 2017 sediments of a marine mangrove in the Caribbean. TEM shows that this new isolate contains Accepted after revision 17 July 2018 intracytoplasmic vesicular membrane systems (containing bacteriochlorophyll a) and larger Available online 7 August 2018 internal sulfur granules, confirmed by EDXS analyses performed using ESEM. The sulfur distribution and mapping obtained for this PSB strain has allowed us to conclude that elemental Keywords: sulfur is formed as an intermediate oxidation product and stored intracellularly. SEM shows Chromatiaceae that the bacterial cells are ovoid and extremely motile via lophotrichous flagella. Phylogenetic Anoxygenic phototrophs characterization, based on the analysis of 16S rDNA and functional gene pufM sequences, Photosynthetic pigment demonstrate that this strain belongs to the Chromatiaceae and may be a representative of a new Gene pufM Phylogeny species of the genus Halochromatium. Thus, reduced sediments of marine mangrove represent a Ultrastructure sulfide-rich environment that sustains the development of Chromatiaceae, in addition to sulfur- EDX oxidizing bacteria and cyanobacteria, as previously reported. C 2018 Published by Elsevier Masson SAS on behalf of Acade´mie des sciences. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/ by-nc-nd/4.0/). R E´ S U M E´ Mots cle´s : Ce travail de´crit une bacte´rie sulfureuse pourpre marine (PSB) re´colte´e au niveau des Chromatiaceae mangroves de bord de mer de la Caraı¨be. Des analyses ultrastructurales ont montre´ que les Phototrophes anoxyge´niques bacte´ries sont ovoı¨des et posse`dent des flagelles de distribution lophotriche. De plus, il existe Pigments photosynthe´tiques des syste`mes membranaires ve´siculaires intra cytoplasmiques (contenant de la bacte´rio- Ge`ne pufM chlorophylle a) et des granules internes de soufre identifie´s par analyse EDXS a` l’aide d’un Phyloge´nie ´ ´ ´ Ultrastructure microscope electronique environnemental. La cartographie du soufre elementaire montre EDX qu’il est stocke´ a` l’inte´rieur des cellules bacte´riennes. La caracte´risation phyloge´ne´tique, * Corresponding author. De´partement de Biologie, UFR SEN, BP 592, 97159 Pointe-a`-Pitre, Guadeloupe. E-mail address: [email protected] (O. Gros). https://doi.org/10.1016/j.crvi.2018.07.001 C 1631-0691/ 2018 Published by Elsevier Masson SAS on behalf of Acade´mie des sciences. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 388 O. Gros et al. / C. R. Biologies 341 (2018) 387–397 base´e sur l’analyse de l’ADNr 16S et du ge`ne de fonction pufM, sugge`re que cette souche appartient aux Chromatiaceae et pourrait repre´senter une nouvelle espe`ce du genre Halochromatium. Ainsi, les se´diments marins re´duits de mangrove repre´sen- tent un environnement riche en sulfures permettant le de´veloppement de Chromatiaceae, en plus des bacte´ries sulfo-oxydantes et des cyanobacte´ries pre´ce´demment de´crites. C 2018 Publie´ par Elsevier Masson SAS au nom de Acade´mie des sciences. Cet article est publie´ en Open Access sous licence CC BY-NC-ND (http://creative- commons.org/licenses/by-nc-nd/4.0/). 1. Introduction non-cultivable and molecular analyses can be comple- mented by ultrastructural analyses coupled with X-ray For most, mangroves simply represent large areas of analysis to detect the elemental sulfur inside the cells [15]. trees that mainly occur in the intertidal zone, between land PSB belong to the order Chromatiales (class Gam- and sea, in the tropics. On the marine border, this ecosystem maproteobacteria), which contains four families, two is characterized by ‘‘normal’’ seawater with pH, tempera- of them are phototrophic: the Chromatiaceae and the ture, salinity, and dissolved oxygen similar to that of other Ectothiorhodospiraceae. The major phenotypic difference tropical marine environments. Most studies have focused on between these two families concerns the localization of the terrestrial zone of the mangrove, and very few have sulfur, internal versus external sulfur granules, respec- analyzed the prokaryotes colonizing marine sediments in tively. The members of Chromatiaceae belong to three this ecosystem. Microbial mats in mangrove tidal channels phylogenetic groups: (1) marine and halophilic species often have an outer layer of cyanobacteria and inner layers comprising the genera Halochromatium, Isochromatium, composed of anoxygenic phototrophic bacteria [1,2]. and Marichromatium (2) freshwater species belonging to Bacterial cells colonizing aquatic sediments are gener- the genera Chromatium and Thiocystis, and (3) water/mud ally organized, based on their physiology, in a vertical axis from freshwater to marine species of the genera Thiocapsa forming a laminated structure. The top layer is usually and Amoebobacter [16]. dominated by a filamentous cyanobacteria species and Anoxygenic photolithotrophic bacteria use reduced benthic diatoms followed by a distinct layer of anoxygenic sulfur species as an electron source [17] to grow. Thus, phototrophs (purple and green bacteria). White patches of the sulfides, produced in the mangrove sediments by filamentous colorless sulfur-oxidizing bacteria, belonging sulfate-reducing bacteria (SRB), diffuse upward into the to Beggiatoaceae, can occasionally be observed at the bottom waters and can be used by anoxygenic photo- surface of the marine sediment [3,4]. These first upper trophic bacteria. In mangroves, anoxygenic photosynthetic layers are followed by sulfate-reducing bacteria, which are bacteria, including purple sulfur bacteria (Chromatium responsible for producing sulfides under anaerobic condi- spp.) and purple non-sulfur bacteria (Rhodopseudomonas tions, which can reach up to 20 mM in marine mangrove spp.), have been isolated from terrestrial mangrove soils in sediments [5]. Pichavaram, South India [18–20]. However, there is no Anoxygenic photolithotrophic bacteria belong to the description available from the literature concerning PSB in categories of green sulfur bacteria (GSB) and purple sulfur marine mangrove sediments. bacteria (PSB), which can form clearly visible colored Here, we explored the contribution of PSB to marine microbial mats in various natural and/or anthropogenical- mangrove microbial communities using phylogenetic ly influenced environments [6]. Purple bacteria can also be analyses (the 16S rRNA gene and the PufM subunit of permanently exposed to oxygen at the sediment surface, as the photosynthetic reaction center) coupled with ultra- observed during mass development of PSB in intertidal structural investigations (ESEM, TEM, EDXS) and FISH zones [7–10]. experiments to characterize and identify these dominant PSB in anaerobic aquatic environments perform anaer- anoxygenic phototrophic bacteria from this tropical obic and anoxygenic photosynthesis, in contrast to marine environment. cyanobacteria [11]. They do not use water as a reducing agent and thus do not produce oxygen. They oxidize 2.
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