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Anaerobic endosymbiont generates energy for ciliate host by denitrification.

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 endosymbiosis^1,2. 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.

SUBMITTER: Graf JS

PROVIDER: S-EPMC7969357 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Simple Summary Rare organisms represent a challenge for researchers in all fields of study in biology. In the realm of ciliatology, the genera Dactylochlamys and Legendrea are considered to be such cases. Very little information has accrued in over a century since their first descriptions; only a few published reports, online images or videos of rarely encountered individual specimens exist. Dactylochlamys and Legendrea are also morphologically remarkable for their likely independently evolved tentacle-like structures. Recently, the first molecular data were published for the species L. loyezae. In our study, we present more robust phylogenetic analysis based on three molecular markers of Dactylochlamys pisciformis and all of the three known Legendrea species, showing that they likely represent a new anaerobic lineage of ciliates. We first provide a detailed morphological characterization of both genera using modern microscopy and staining methods. We identify and discuss the bacterial (Syntrophaceae) and archaeal endosymbionts harbored by both genera based on 16S rRNA gene sequences. We also discovered that Legendrea preys on gastrotrichs, which is supported by molecular data and a unique video material documenting the feeding behavior of one Legendrea species. This study brings essential information needed to better understand the phylogeny, life strategies, and rarity of these organisms and emphasizes the importance of citizen science. Abstract Free-living anaerobic ciliates are of considerable interest from an ecological and an evolutionary standpoint. Extraordinary tentacle-bearing predatory lineages have evolved independently several times within the phylum Ciliophora, including two rarely encountered anaerobic litostomatean genera, Legendrea and Dactylochlamys. In this study, we significantly extend the morphological and phylogenetic characterization of these two poorly known groups of predatory ciliates. We provide the first phylogenetic analysis of the monotypic genus Dactylochlamys and the three valid species of Legendrea based on the 18S rRNA gene and ITS-28S rRNA gene sequences. Prior to this study, neither group had been studied using silver impregnation methods. We provide the first protargol-stained material and also a unique video material including documentation, for the first time, of the hunting and feeding behavior of a Legendrea species. We briefly discuss the identity of methanogenic archaeal and bacterial endosymbionts of both genera based on 16S rRNA gene sequences, and the importance of citizen science for ciliatology from a historical and contemporary perspective.

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Anaerobic endosymbiont generates energy for ciliate host by denitrification.

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