Genomics of New Ciliate Lineages Provides Insight into the Evolution of Obligate Anaerobiosis
Summary: Oxygen plays a crucial role in energetic metabolism of most eukaryotes. Yet adaptations to low-oxygen concentrations leading to anaerobiosis have independently arisen in many eukaryotic lineages, resulting in a broad spectrum of reduced and modified mitochondrion-related organelles (MROs). In this study, we present the discovery of two new classlevel lineages of free-living marine anaerobic ciliates, Muranotrichea, cl. nov. and Parablepharismea, cl. nov., that, together with the class Armophorea, form a major clade of obligate anaerobes (APM ciliates) within the Spirotrichea, Armophorea, and Litostomatea (SAL) group. To deepen our understanding of the evolution of anaerobiosis in ciliates, we predicted the mitochondrial metabolism of cultured representatives from all three classes in the APM clade by using transcriptomic and metagenomic data and performed phylogenomic analyses to assess their evolutionary relationships. The predicted mitochondrial metabolism of representatives from the APM ciliates reveals functional adaptations of metabolic pathways that were present in their last common ancestor and likely led to the successful colonization and diversification of the group in various anoxic environments. Furthermore, we discuss the possible relationship of Parablepharismea to the uncultured deep-sea class Cariacotrichea on the basis of single- gene analyses. Like most anaerobic ciliates, all studied species of the APM clade host symbionts, which we propose to be a significant accelerating factor in the transitions to an obligately anaerobic lifestyle. Our results provide an insight into the evolutionary mechanisms of early transitions to anaerobiosis and shed light on fine-scale adaptations in MROs over a relatively short evolutionary time frame
Rotterová J., Salomaki E., Pánek T., Bourland W., Žihala D., Táborský P., Edgcomb V.P., Beinart R.A., Kolísko M., Čepička I. 2020: Genomics of new ciliate lineages provides insight into the evolution of obligate anaerobiosis. Current Biology (in press). [IF=9.193]
DOI: 10.1016/j.cub.2020.03.064
Highlights
- Discovery and cultivation of two new classes of marine ciliates thriving in anoxia
- Phylogenomics reveals a major clade of obligate anaerobes in ciliates
- Novel insights into evolution of mitochondrial metabolism in anaerobic eukaryotes
- Transitions to obligate anaerobiosis might be facilitated by prokaryotic symbionts
Keywords
anoxia, mitochondria, metagenome, MRO´s, phylogenomics, protistst, ranscriptome, anaerobiosis, ciliates, symbiosis
Introduction
Anaerobic eukaryotes have long intrigued biochemists and evolutionary biologists, as free oxygen is widely considered essential for life in this domain. Among other functions in the cell, oxygen plays a crucial role as a terminal electron acceptor in mitochondrial ATP production via oxidative phosphorylation. Yet numerous eukaryotic lineages have adapted to low-oxygen concentrations and thrive in hypoxic or even anoxic environments [1]. Although some of them are still able to survive exposure to oxygen, others are obligate anaerobes whose mitochondria have been reduced to various forms of mitochondrion-related organelles (MROs). Depending on the completeness of the electron transport chain (ETC) and the organism’s resulting type of energetic metabolism, as well as other retained and gained mitochondrial functions, MROs are traditionally classified into several categories: anaerobic mitochondria; hydrogen-producing mitochondria; hydrogenosomes; and mitosomes [2, 3]. However, it is now accepted that MROs exist in a functional and evolutionary continuum without sharp borders between categories [1, 4, 5, 6, 7]. One extreme in this spectrum is the complete loss of the mitochondrion, as recently documented in the flagellate Monocercomonoides (Metamonada) [8]. Although comparative studies of highly reduced MRO forms are important for our understanding of the minimum requirements for cell function and energy production, they do not provide insight into the early stages of adaptation to anoxia [1].
DOI: 10.1016/j.cub.2020.03.064
