Abstract

Mitochondria are specialized eukaryotic organelles that have a dedicated function in oxygen respiration and energy production. They evolved about 2 billion years ago from a free-living bacterial ancestor (probably an alphaproteobacterium), in a process known as endosymbiosis1,2. Many unicellular eukaryotes have since adapted to life in anoxic habitats and their mitochondria have undergone further reductive evolution3. As a result, obligate anaerobic eukaryotes with mitochondrial remnants derive their energy mostly from fermentation4. Here we describe ‘Candidatus Azoamicus ciliaticola’, which is an obligate endosymbiont of an anaerobic ciliate and has a dedicated role in respiration and providing energy for its eukaryotic host. ‘Candidatus A. ciliaticola’ contains a highly reduced 0.29-Mb genome that encodes core genes for central information processing, the electron transport chain, a truncated tricarboxylic acid cycle, ATP generation and iron–sulfur cluster biosynthesis. The genome encodes a respiratory denitrification pathway instead of aerobic terminal oxidases, which enables its host to breathe nitrate instead of oxygen. ‘Candidatus A. ciliaticola’ and its ciliate host represent an example of a symbiosis that is based on the transfer of energy in the form of ATP, rather than nutrition. This discovery raises the possibility that eukaryotes with mitochondrial remnants may secondarily acquire energy-providing endosymbionts to complement or replace functions of their mitochondria.

Highlights

  • Some eukaryotes that inhabit anoxic environments do not contain aerobic mitochondria

  • We observed a high abundance of motile unicellular eukaryotes throughout the anoxic layer (Fig. 1, Extended Data Fig. 1, Supplementary Video 1)

  • A substantial fraction of the ciliates observed in the anoxic hypolimnion contained multiple intracellular DAPI signals that were reminiscent of endosymbionts

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Summary

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Mitochondria are specialized eukaryotic organelles that have a dedicated function in oxygen respiration and energy production. They evolved about 2 billion years ago from a free-living bacterial ancestor (probably an alphaproteobacterium), in a process known as endosymbiosis[1,2]. We describe ‘Candidatus Azoamicus ciliaticola’, which is an obligate endosymbiont of an anaerobic ciliate and has a dedicated role in respiration and providing energy for its eukaryotic host. ‘Candidatus A. ciliaticola’ and its ciliate host represent an example of a symbiosis that is based on the transfer of energy in the form of ATP, rather than nutrition This discovery raises the possibility that eukaryotes with mitochondrial remnants may secondarily acquire energy-providing endosymbionts to complement or replace functions of their mitochondria. We report the discovery of an obligate endosymbiont of an anaerobic ciliate that provides its host with energy derived from denitrification

Anaerobic ciliates with bacterial endosymbionts
MAC e f
Endosymbiont and host phylogeny
Bacterial genome with endosymbiotic features
Number of ciliates per litre
Anaerobic respiration and energy metabolism
Putative intermediate stage
Evolution of the respiratory symbiosis
Online content
Methods
Probe design for fluorescence in situ hybridization
Metagenome and bulk metatranscriptome sequencing
Genome assembly and finishing
Metatranscriptomic analyses of bulk water samples
Phylogenetic analyses
Incubation experiments
Findings
Statistics and reproducibility
Full Text
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