methanogen endosymbionts also utilise CO 2 derived from the ciliate’s digestion of prey.
Methanogens were some of the first endosymbionts of anaerobic ciliates to have their genomes sequenced and analysed. These studies revealed that their genomes are similar in size to their free-living methanogen relatives, in contrast to many bacterial endosymbionts in other eukaryote hosts that often have undergone substantial genome reduction. Nevertheless, at least some methanogen endosymbionts have lost genes for the biosynthesis of several amino acids, suggesting that they have become obligate symbionts that are dependent on their ciliate hosts for providing some of their essential organic molecules. Several methanogen-containing anaerobic ciliates, including Trimyema compressum , Metopus striatus and Cyclidium spp., also have endosymbiotic bacteria. These represent some of the few known cases of both archaea and bacteria living stably within eukaryote cells. These complex consortia indicate further development of metabolic partnerships; however, as yet we know little about the bacterial partners in these consortia including interactions between the prokaryote symbionts or either with their hosts. Ciliates with green algae and purple bacteria endosymbionts A further complex symbiotic consortium is found in the ciliate Pseudoblepharisma tenue that has two endosymbionts; one a purple Gammaproteobacteria capable of anoxygenic photosynthesis and the other a green algae eukaryote capable of oxygenic photosynthesis (Figure 2). The combined metabolisms of these separate symbiotic partners create a complex mixotrophic physiological niche for the ciliate, yet also make it somewhat flexible in oxic/anoxic habitat choice. Comparative genomic analysis of these three symbiotic partners suggests that each can switch between anaerobic and aerobic metabolic pathways depending on the availability of oxygen. P. tenue is not an anaerobic ciliate in the strictest sense since it appears to have aerobic mitochondria, rather than hydrogenosomes, that likely require oxygen to perform oxidative phosphorylation. The two endosymbionts adapt their metabolisms between photosynthetic and non-photosynthetic fermentative or respiratory metabolic pathways, depending on the availability of light. In the dark, it is likely that the ciliate prefers to occupy an aerobic environment so that all three symbiotic partners can utilise their more efficient aerobic respiratory pathways, rather than their fermentative anaerobic pathways. However, when light is present, it is likely that the
Figure 2. Purple Gammaproteobacteria and Chlorella green algae endosymbionts in the freshwater ciliate Pseudoblepharisma tenue . Martin Kreutz
ciliate moves between both oxic and anoxic environments, to provide both its endosymbionts with opportunities to photosynthesise. Thus, P. tenue occupies the oxic–anoxic boundary regions of the freshwater ponds in which it is found. Moreover, its anoxygenic photosynthesising bacterial endosymbionts likely enable it to ‘SCUBA-dive’ into deeper anoxic environments, providing opportunities to access alternative sources of microbial prey. Genomics-based metabolic reconstruction enabled further inferences of the biochemical basis for the interaction between these separate partners. It seems possible that the ciliate provides the bacterial endosymbionts with organic compounds, in the form of acetate and propionate, and nitrogen in the form of ammonium. In exchange, the photosynthesis of the bacteria fixes CO 2 , making small inorganic molecules that it might export as an alternative source of organic carbon for the ciliate. There are other described anaerobic ciliates with purple photosynthetic bacterial endosymbionts, and these might provide insights into the intermediate stages of development of the three-way partnership seen in P. tenue . However, as for P. tenue , none have been successfully brought into culture, creating a barrier to experimental investigation of these complex symbiotic systems. Ciliates with endosymbiotic nitrate-respiring bacteria with similarities to mitochondria An anaerobic plagiopylean ciliate recently discovered from the deep anoxic water layers of Lake Zug in Switzerland has the only known example of an endosymbiont capable of anaerobic respiration using nitrate as a terminal electron acceptor. Molecular analysis suggests that ATP is produced by nitrate respiration in the endosymbiont. This could be exported to the ciliate and, if so, would be equivalent to mitochondrial export of ATP as the product of aerobic (oxygen) respiration.
86 Microbiology Today October 2022 | microbiologysociety.org
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