Close Interspecies Interactions between Prokaryotes from Sulfureous Environments

Abstract

Green sulfur bacteria are obligate photolithoautotrophs that require highly reducing conditions for growth and can utilize only a very limited number of carbon substrates. These bacteria thus inhabit a very narrow ecologic niche. However, several green sulfur bacteria have overcome the limits of immobility by entering into a symbiosis with motile Betaproteobacteria in a type of multicellular association termed phototrophic consortia. One of these consortia, “Chlorochromatium aggregatum,” has recently been established as the first culturable model system to elucidate the molecular basis of this symbiotic interaction. It consists of 12–20 green sulfur bacteria epibionts surrounding a central, chemoheterotrophic betaproteobacterium in a highly ordered fashion. Recent genomic, transcriptomic, and proteomic studies of “C. aggregatum” and its epibiont provide insights into the molecular basis and the origin of the stable association between the two very distantly related bacteria. While numerous genes of central metabolic pathways are upregulated during the specific symbiosis and hence involved in the interaction, only a limited number of unique putative symbiosis genes have been detected in the epibiont. Green sulfur bacteria therefore are preadapted to a symbiotic lifestyle. The metabolic coupling between the bacterial partners appears to involve amino acids and highly specific ultrastructures at the contact sites between the cells. Similarly, the interaction in the equally well studied archaeal consortia consisting of Nanoarchaeum equitans and its host Ignicoccus hospitalis is based on the transfer of amino acids while lacking the highly specialized contact sites observed in phototrophic consortia.

Metabolic analysis of Chlorobium chlorochromatii CaD3 reveals clues of the symbiosis in ‘Chlorochromatium aggregatum’

“…This would facilitate the diffusion of 2-oxoglutarate from the central bacterium to the chlorobia. However, recent experiments suggest that the proposed periplasmic space is not a place where molecules can freely diffuse (Mü ller and Overmann, 2011). Anyway, it has been shown that Chl.…”

“…Several lines of evidence suggest that the b-proteobacterium and not the chlorobia, assimilates this metabolite from the medium (Frö stl and Overmann et al, 1998;Glaeser and Overmann, 2003b;Vogl et al, 2006). However, it is not known whether the central bacterium transfers organic carbon to the epibiont (Mü ller and Overmann, 2011). Previous studies analyzed the D 13 C ratio (that is, the difference between the d 13 C values of biomarkers and the d 13 C of ambient) to elucidate the carbon source used by the epibionts in 'P.…”

“…CO 2 is fixed via the reverse tricarboxylic acid cycle (rTCA) (Vogl et al, 2006). In natural conditions they are exclusively found in symbiosis although they can be cultured without their symbiont, which is not the case for the obligate-symbiotic b-proteobacterium (Mü ller and Overmann, 2011). Previous studies have identified genes that code for virulence factors in Chl.…”

Evolution of microbial markets

“…In a mutualism between sulfur-reducing, chemotrophic bacteria and phototrophic sulphide oxidizers, spatially organized aggregates called consortia are formed (56,57), potentially allowing for more controlled resource flow (56,58). Likewise, cross-feeding mutualisms between hydrogen-producing fermenters and methanogens (e.g., in sewage sludge) form aggregative flocs to retain shared metabolites (54).…”

Genomic analysis reveals key aspects of prokaryotic symbiosis in the phototrophic consortium “Chlorochromatium aggregatum”

“…Flagella-powered taxis towards sulfide and away from darkness towards light - which are the main energy and electron sources of GSB - would allow consortia to adjust more quickly to fluctuating light and oxygen conditions during the diel cycle in their natural habitats [34]. Diel vertical migration behavior is highly advantageous for the flagellated purple sulfur bacterium Chromatium minus [48], and directed motility is generally regarded as one of the major advantages that allow phototrophic consortia to outcompete free-living GSB [49]. …”