Love knows no oxic–anoxic boundaries: anaerobiosis in ciliates provides rich opportunities for microbial symbiosis
William H. Lewis and Ross F. Waller
The diversity of anaerobic life and the environments where it is found
Ciliates are anoxia specialists with a proclivity for hosting symbionts Ciliates are one group of eukaryotes that have been
We often think of our planet as an oxygenated habitat, but anoxic environments are relatively widespread on Earth. They most often occur where there is an accumulation of dead organic material and the diffusion of oxygen is limited. Such environments include the deeper aquatic layers and sediments of ponds, lakes and oceans, as well as the digestive tracts of many animals. These environments provide habitats for highly diverse anaerobic microbial communities that thrive in low- or no-oxygen conditions and, therefore, produce energy using metabolic pathways independent of oxygen. Highly diverse metabolisms have evolved over billions of years in prokaryotes to generate energy from a range of different substrates in these anoxic environments. These include different types of fermentation, as well as different forms of anaerobic respiration using electron transport chains with alternative terminal electron acceptors to oxygen. Living alongside the prokaryotes in anoxic environments there are also anaerobic microbial eukaryotes (protists) that evolved more recently from aerobic eukaryote ancestors. This transition from aerobe to anaerobe has occurred in several protist groups in parallel, for example in metamonads, amoebozoans, stramenopiles, rhizarians and ciliates. The transition to anaerobe is typically achieved by transforming aerobic mitochondria into hydrogen-producing anaerobic versions called hydrogenosomes. Hydrogenosomes lack key mitochondrial metabolic pathways, most notably the electron transport chain for oxidative phosphorylation. Instead, they make ATP by oxygen-independent fermentation reactions and substrate phosphorylation, with molecular hydrogen as a by-product. In actuality, aerobic mitochondria and hydrogenosomes can be considered as two extreme states on a spectrum of mitochondrial adaptation to anoxia, with examples across this spectrum found widely in different protist lineages.
particularly successful at adapting to anoxic environments. At least 15 ciliate lineages have independently undergone the transition from aerobe, with canonical mitochondria, to anaerobe with hydrogenosomes (or hydrogen-producing mitochondria) – more times than any other eukaryotic group. A key to the success of ciliates in making this transition is their FeFe-hydrogenase, which is responsible for hydrogen production during energy metabolism. The ciliate version of this enzyme has an unusual and characteristic domain structure including an additional two bacterial-like NADH-dehydrogenase domains at the C-terminus. But more surprising is phylogenetic evidence for the different anaerobic ciliate lineages having inherited this enzyme vertically from their aerobic forebears. This is surprising as FeFe-hydrogenases require anoxic conditions to function and are inhibited by oxygen, so their purpose in aerobic ciliates is unclear. Nevertheless, this ancestry does provide a rationale for why multiple independent developments of anaerobic lifestyles have occurred in ciliates – they already had some key kit for the transition. A second reason for the metabolic flexibility of ciliates is that many host microbial endosymbionts. There are probably two main features of ciliate cells that promote this proclivity for symbiosis. The first is their cell size; ciliates can be huge, ranging from 10 µm to 4 mm in length. Many ciliates, therefore, have large cell volumes that provide ample space to host numerous smaller endosymbiont cells. The second feature is that ciliates are predators that feed by phagotrophy, engulfing large numbers of microbial cells that are digested in food vacuoles. This regular internalisation of diverse microbial cells likely increases the chance of a microbe finding its way into the ciliate cytoplasm, with escape from a food vacuole being more probable than invading across the outer layers of a eukaryotic cell. Thus, the frequency of ciliates encountering novel potential
84 Microbiology Today October 2022 | microbiologysociety.org
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