Microbiology Today October 2022: Protists

The ancestors of modern-day mitochondria were also endosymbiotic bacteria, a partnership that was seminal to the origin of all eukaryotes. The endosymbionts in the ciliate from Lake Zug have, therefore, been proposed as a possible modern- day anaerobic analogy for mitochondria. Understanding this new ciliate symbiosis could elucidate common biological processes relevant to the initial establishment of mitochondria, an event so ancient that it is almost impossible to otherwise investigate. The Lake Zug ciliate is a remarkable case of the reintroduction of respiration into a eukaryote that had lost it. The ciliate retains fermentative ATP-producing hydrogenosomes, so presumably ATP produced from the nitrate respiration of the symbiont is not sufficient for outright loss of this anaerobic mitochondrial relict. But in the endosymbiont, multiple biosynthesis pathways for essential molecules such as nucleotides, phospholipids and lipopolysaccharides have been lost. So, the symbiont is dependent on its ciliate host and these are the hallmarks of an already well-integrated partnership. As with each of the ciliates discussed, much more could be learned about the ciliate from Lake Zug if it could be cultivated. Whilst there has been much success culturing numerous anaerobic ciliates that have methanogen endosymbionts, those with more novel endosymbionts have proved more difficult. This could reflect their more complex, or less well understood metabolic requirements, which are more difficult to identify and replicate in a laboratory culture setting. However, the prize for overcoming this hurdle is potentially great, as cultivation opens the door to a range of experimental techniques that can provide far deeper insights into the interactions between these fascinating and intricately associated microbes. In any case, ciliates already demonstrate the possibilities that microbial symbioses offer, and where the challenges of oxic–anoxic boundaries can in fact become opportunities for new niches to exploit. Further Reading Graf JS, Schorn S, Kitzinger K, Ahmerkamp S, Woehle C et al. Anaerobic endosymbiont generates energy for ciliate host by denitrification. Nature 2021;591:445–450. Lewis WH, Lind AE, Sendra KM, Onsbring H, Williams TA et al. Convergent evolution of hydrogenosomes from mitochondria by gene transfer and loss. Mol Biol Evol 2020;37:524–539. Lind AE, Lewis WH, Spang A, Guy L, Embley TM et al. Genomes of two archaeal endosymbionts show convergent adaptations to an intracellular lifestyle. ISME J 2018;12:2655–2667.

Muñoz-Gómez SA, Kreutz M, Hess S. A microbial eukaryote with a unique combination of purple bacteria and green algae as endosymbionts. Sci Adv 2021;7:eabg4102. Rotterová J, Edgcomb VP, Čepička I, Beinart R. Anaerobic ciliates as a model group for studying symbioses in oxygen-depleted environments. J Eukaryot Microbiol 2022;e12912. Acknowledgements We would like to thank the Gordon and Betty Moore Foundation Symbiosis in Aquatic Systems Initiative for their support.

About the authors

William H. Lewis Postdoctoral Researcher, Department of Biochemistry, University of Cambridge, UK

whl30@cam.ac.uk @WillLew12

William completed his PhD at Newcastle University, UK, in 2017, followed by a postdoc at Wageningen University, Netherlands, before moving to Cambridge.

Ross F. Waller Professor of Evolutionary Cell Biology, Department of Biochemistry, University of Cambridge, UK.

rfw26@cam.ac.uk wallercellevolution.com @RossWaller3

Why does microbiology matter? Will: Microbes form the vast majority of life on Earth and have evolved diverse forms, colonising essentially every environment that exists on our planet. Without microbiology, how can we even begin to understand and appreciate the living world around us? Could you describe one of your typical workdays? Will: Currently, my typical workday is comprised of growing algal cultures and performing experiments on these in the lab, as well as analysing transcript or protein data from these organisms computationally, normally using mostly Linux-based tools. My current work aims to understand the evolution and integration of plastids and photosynthetic endosymbionts that have evolved independently in several different species of dinoflagellates.

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