Close Interspecies Interactions Between Prokaryotes from Sulfureous Environments

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Close Interspecies Interactions Between Prokaryotes from Sulfureous Environments REVIEW ARTICLE published: 05 July 2011 doi: 10.3389/fmicb.2011.00146 Close interspecies interactions between prokaryotes from sulfureous environments Johannes Müller† and Jörg Overmann†∗ Bereich Mikrobiologie, Department Biologie I, Ludwig-Maximilians-Universität München, Planegg-Martinsried, Germany Edited by: Green sulfur bacteria are obligate photolithoautotrophs that require highly reducing con- Thomas E. Hanson, University of ditions for growth and can utilize only a very limited number of carbon substrates. These Delaware, USA bacteria thus inhabit a very narrow ecologic niche. However, several green sulfur bac- Reviewed by: Jennifer Macalady, Pennsylvania teria have overcome the limits of immobility by entering into a symbiosis with motile State University, USA Betaproteobacteria in a type of multicellular association termed phototrophic consortia. James T. Hollibaugh, University of One of these consortia, “Chlorochromatium aggregatum,” has recently been established Georgia, USA as the first culturable model system to elucidate the molecular basis of this symbiotic *Correspondence: interaction. It consists of 12–20 green sulfur bacteria epibionts surrounding a central, Jörg Overmann, Leibniz-Institut, Deutsche Sammlung von chemoheterotrophic betaproteobacterium in a highly ordered fashion. Recent genomic, Mikroorganismen und Zellkulturen, transcriptomic, and proteomic studies of “C. aggregatum” and its epibiont provide insights Inhoffenstraße 7B, 38124 into the molecular basis and the origin of the stable association between the two very Braunschweig, Germany. distantly related bacteria. While numerous genes of central metabolic pathways are upreg- e-mail: [email protected] †Present address: ulated during the specific symbiosis and hence involved in the interaction, only a limited Johannes Müller and Jörg Overmann, number of unique putative symbiosis genes have been detected in the epibiont. Green Leibniz-Institut, Deutsche Sammlung sulfur bacteria therefore are preadapted to a symbiotic lifestyle. The metabolic coupling von Mikroorganismen und Zellkulturen Braunschweig and between the bacterial partners appears to involve amino acids and highly specific ultra- Technical University of Braunschweig, structures at the contact sites between the cells. Similarly, the interaction in the equally Inhoffenstraße 7B, 38124 well studied archaeal consortia consisting of Nanoarchaeum equitans and its host Ignicoc- Braunschweig, Germany. cus hospitalis is based on the transfer of amino acids while lacking the highly specialized contact sites observed in phototrophic consortia. Keywords: Chlorochromatium aggregatum, phototrophic consortia, symbiosis, green sulfur bacteria, Ignicoccus hospitalis, Nanoarchaeum equitans INTRODUCTION substrates, they profit energetically from the rapid consumption In their natural environment, planktonic bacteria reach total cell of their excretion products. This renders their metabolism ener- numbers of 106 ml–1, whereas in sediments and soils, 109 and 1011 getically more favorable or makes some reactions even possible bacterial cells·cm–3, respectively, have been observed (Fægri et al., (Bryant, 1979; Zehnder et al., 1982; McInerney, 1986; Schink, 1977; Whitman et al., 1998). Assuming a homogenous distribu- 1992). Recent studies of syntrophic communities in Lake Con- tion,distances between bacterial cells in these environments would stance profundal sediments yielded new and unexpected results. amount to 112 μm for planktonic, 10 μm for sediment envi- The dominant sugar-degrading bacteria were not the typical fer- ronments and about 1 μm for soil bacteria (Overmann, 2001b). menting bacteria that dominate in anaerobic sludge systems or Taking into account the estimated number of bacterial species the rumen environment. They rather represented syntrophic bac- in soil that range from 500,000 (Dykhuizen, 1998)to8.3×106 teria most closely related to the genus Bacillus that could only be (Gans et al., 2005), the closest neighbors of each cell statistically grown anaerobically and in coculture with the hydrogen-using should represent different species. A spatially close association of methanogen Methanospirillum hungatei (Müller et al., 2008). different bacterial species can result in metabolic complementa- For efficient syntrophic substrate oxidation, close physical con- tion or other synergisms. In this context, the most extensively tact of the partner organisms is indispensable. Monocultures of studied example is the conversion of cellulose to methane and Pelotomaculum thermopropionicum strain SI and Methanother- carbon dioxide in anoxic habitats. The degradation is only pos- mobacter thermautotrophicus show dispersed growth of the cells. sible by a close cooperation of at least four different groups of In contrast, cocultures of the two strains formed tight aggregates bacteria that encompass primary and secondary fermenting bac- when grown on propionate, for which the allowed distance for teria as well as two types of methanogens. Along this anaerobic syntrophic propionate oxidation was estimated to be approxi- food chain, end products of one group are exploited by the mem- mately 2 μm(Ishii et al., 2005). Interestingly, the H2-consuming bers downstream the flow of electrons. Although the bacteria partner in syntrophic relationships can be replaced by an H2- involved in the first steps of cellulose degradation do not obligately purging culture vessel, allowing Syntrophothermus lipocalidus to depend on the accompanying bacteria for provision of growth grow on butyrate and Aminobacterium colombiense on alanine in www.frontiersin.org July 2011 | Volume 2 | Article 146 | 1 Müller and Overmann Bacterial interspecies interactions pure culture (Adams et al.,2006). Thus,the syntrophic associations (Glaeser and Overmann,2003b).Within the Betaproteobacteria the investigated to date are typically based on efficient H2-removal as central bacterium represents a so far isolated phylogenetic lineage obligate basis for their interdependence. Additional types of bac- belonging to the family of the Comamonadaceae. The closest rel- terial interactions have been described more recently. Cultures of atives are Rhodoferax spp., Polaromonas vacuolata and Variovorax Pseudomonas aeruginosa were shown to only grow on chitin if paradoxus (Kanzler et al., 2005). in coculture with a chitin degrading bacterium like Aeromonas Based solely on their morphology, 10 different phototrophic hydrophila. In addition to simply growing on the degradation consortia can be distinguished to date (Overmann, 2001a; Over- products produced by the exoenzymes of the partner, P. aerugi- mann and Schubert, 2002). The majority of the morphotypes are nosa induced release of acetate in A. hydrophila by inhibiting its motile,motility being conferred by the central colorless bacterium. aconitase employing pyocyanin. The resulting incomplete oxida- The 13–69 epibiont cells are either green or brown-colored repre- tion of chitin to acetate by A. hydrophila is then exploited by P. sentatives of the green sulfur bacteria. The smaller consortia like aeruginosa foritsowngrowth(Jagmann et al., 2010). “Chlorochromatium aggregatum” (harboring green epibionts) and Although these well-characterized associations certainly are of “Pelochromatium roseum” (brown epibionts), are barrel shaped major ecological relevance in their respective environments, they and consist of 12–20 epibiont cells (Overmann et al., 1998). Rather were typically obtained using standard defined growth media. globular in shape and consisting of ≥40 epibionts are the sig- As a result, presently available laboratory model systems were nificantly larger consortia “Chlorochromatium magnum” (green selected based on their ability to grow readily and – under at epibionts; Fröstl and Overmann, 2000), “Pelochromatium latum” least some experimental conditions – on their own in pure cul- (brown epibionts; Glaeser and Overmann, 2004) and “Pelochro- ture. Obviously, this cultivation strategy counterselects against matium roseo-viride” (Gorlenko and Kusnezow, 1972). The latter bacterial associations of obligately or at least tight interdepen- consortium is the only one harboring two types of epibionts, dence. While the significant advances in the development of with brown cells forming an inner layer and green ones an outer cultivation-independent techniques permit a partial analysis of layer.“Chloroplana vacuolata” and“Cylindrogloea bactifera”can be so-far-uncultured associations (Orphan et al., 2001; Blumenberg distinguished from the other consortia by their immotility and dif- et al., 2004; Pernthaler et al., 2008), laboratory grown model sys- ferent cell arrangement. “Chloroplana vacuolata” consists of rows tems are still indispensable for in-depth studies of gene expression of green sulfur bacteria alternating with colorless bacteria forming and metabolism. One model system of prokaryotic associations a flat sheath (Dubinina and Kuznetsov, 1976), with both species that meanwhile can be grown indefinitely in laboratory culture containing gas vacuoles. In “Cylindrogloea bactifera,” a slime layer is the phototrophic consortium “Chlorochromatium aggregatum.” containing green sulfur bacteria is surrounding filamentous, col- This consortium represents the most highly developed bacteria– orless bacteria (Perfiliev, 1914; Skuja, 1956). Since they consist of bacteria symbiosis known to date. In parallel, the archaea–archaea two different types of bacteria, the names of consortia are with- association between Ignicoccus
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