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 class-level 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.

Department of Biological Sciences Boise State University Boise ID 83725 1515 USA

Department of Biology and Ecology Faculty of Science University of Ostrava Ostrava 710 00 Czech Republic

Department of Geology and Geophysics Woods Hole Oceanographic Institution Woods Hole MA 02543 USA

Department of Zoology Faculty of Science Charles University Prague 128 43 Czech Republic

Graduate School of Oceanography University of Rhode Island Narragansett RI 02882 USA

Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice 370 05 Czech Republic

Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice 370 05 Czech Republic; Department of Molecular Biology and Genetics Faculty of Science University of South Bohemia 370 05 České Budějovice Czech Republic

Citace poskytuje Crossref.org

Divergent marine anaerobic ciliates harbor closely related Methanocorpusculum endosymbionts

Methanogenic symbionts of anaerobic ciliates are host and habitat specific

Rediscovery of Remarkably Rare Anaerobic Tentaculiferous Ciliate Genera Legendrea and Dactylochlamys (Ciliophora: Litostomatea)

Reduced mitochondria provide an essential function for the cytosolic methionine cycle

Evidence for an Independent Hydrogenosome-to-Mitosome Transition in the CL3 Lineage of Fornicates

Gregarine single-cell transcriptomics reveals differential mitochondrial remodeling and adaptation in apicomplexans

Releasing uncurated datasets is essential for reproducible phylogenomics

Anaerobic Fungi: Past, Present, and Future