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Genome Analysis of a Verrucomicrobial Endosymbiont With a Tiny Genome Discovered in an Antarctic Lake

Organic Lake in Antarctica is a marine-derived, cold (−13∘C), stratified (oxic-anoxic), hypersaline (>200 gl(–1)) system with unusual chemistry (very high levels of dimethylsulfide) that supports the growth of phylogenetically and metabolically diverse microorganisms. Symbionts are not well chara...

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Autores principales: Williams, Timothy J., Allen, Michelle A., Ivanova, Natalia, Huntemann, Marcel, Haque, Sabrina, Hancock, Alyce M., Brazendale, Sarah, Cavicchioli, Ricardo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8204192/
https://www.ncbi.nlm.nih.gov/pubmed/34140946
http://dx.doi.org/10.3389/fmicb.2021.674758
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author Williams, Timothy J.
Allen, Michelle A.
Ivanova, Natalia
Huntemann, Marcel
Haque, Sabrina
Hancock, Alyce M.
Brazendale, Sarah
Cavicchioli, Ricardo
author_facet Williams, Timothy J.
Allen, Michelle A.
Ivanova, Natalia
Huntemann, Marcel
Haque, Sabrina
Hancock, Alyce M.
Brazendale, Sarah
Cavicchioli, Ricardo
author_sort Williams, Timothy J.
collection PubMed
description Organic Lake in Antarctica is a marine-derived, cold (−13∘C), stratified (oxic-anoxic), hypersaline (>200 gl(–1)) system with unusual chemistry (very high levels of dimethylsulfide) that supports the growth of phylogenetically and metabolically diverse microorganisms. Symbionts are not well characterized in Antarctica. However, unicellular eukaryotes are often present in Antarctic lakes and theoretically could harbor endosymbionts. Here, we describe Candidatus Organicella extenuata, a member of the Verrucomicrobia with a highly reduced genome, recovered as a metagenome-assembled genome with genetic code 4 (UGA-to-Trp recoding) from Organic Lake. It is closely related to Candidatus Pinguicocccus supinus (163,218 bp, 205 genes), a newly described cytoplasmic endosymbiont of the freshwater ciliate Euplotes vanleeuwenhoeki (Serra et al., 2020). At 158,228 bp (encoding 194 genes), the genome of Ca. Organicella extenuata is among the smallest known bacterial genomes and similar to the genome of Ca. Pinguicoccus supinus (163,218 bp, 205 genes). Ca. Organicella extenuata retains a capacity for replication, transcription, translation, and protein-folding while lacking any capacity for the biosynthesis of amino acids or vitamins. Notably, the endosymbiont retains a capacity for fatty acid synthesis (type II) and iron–sulfur (Fe-S) cluster assembly. Metagenomic analysis of 150 new metagenomes from Organic Lake and more than 70 other Antarctic aquatic locations revealed a strong correlation in abundance between Ca. Organicella extenuata and a novel ciliate of the genus Euplotes. Like Ca. Pinguicoccus supinus, we infer that Ca. Organicella extenuata is an endosymbiont of Euplotes and hypothesize that both Ca. Organicella extenuata and Ca. Pinguicocccus supinus provide fatty acids and Fe-S clusters to their Euplotes host as the foundation of a mutualistic symbiosis. The discovery of Ca. Organicella extenuata as possessing genetic code 4 illustrates that in addition to identifying endosymbionts by sequencing known symbiotic communities and searching metagenome data using reference endosymbiont genomes, the potential exists to identify novel endosymbionts by searching for unusual coding parameters.
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spelling pubmed-82041922021-06-16 Genome Analysis of a Verrucomicrobial Endosymbiont With a Tiny Genome Discovered in an Antarctic Lake Williams, Timothy J. Allen, Michelle A. Ivanova, Natalia Huntemann, Marcel Haque, Sabrina Hancock, Alyce M. Brazendale, Sarah Cavicchioli, Ricardo Front Microbiol Microbiology Organic Lake in Antarctica is a marine-derived, cold (−13∘C), stratified (oxic-anoxic), hypersaline (>200 gl(–1)) system with unusual chemistry (very high levels of dimethylsulfide) that supports the growth of phylogenetically and metabolically diverse microorganisms. Symbionts are not well characterized in Antarctica. However, unicellular eukaryotes are often present in Antarctic lakes and theoretically could harbor endosymbionts. Here, we describe Candidatus Organicella extenuata, a member of the Verrucomicrobia with a highly reduced genome, recovered as a metagenome-assembled genome with genetic code 4 (UGA-to-Trp recoding) from Organic Lake. It is closely related to Candidatus Pinguicocccus supinus (163,218 bp, 205 genes), a newly described cytoplasmic endosymbiont of the freshwater ciliate Euplotes vanleeuwenhoeki (Serra et al., 2020). At 158,228 bp (encoding 194 genes), the genome of Ca. Organicella extenuata is among the smallest known bacterial genomes and similar to the genome of Ca. Pinguicoccus supinus (163,218 bp, 205 genes). Ca. Organicella extenuata retains a capacity for replication, transcription, translation, and protein-folding while lacking any capacity for the biosynthesis of amino acids or vitamins. Notably, the endosymbiont retains a capacity for fatty acid synthesis (type II) and iron–sulfur (Fe-S) cluster assembly. Metagenomic analysis of 150 new metagenomes from Organic Lake and more than 70 other Antarctic aquatic locations revealed a strong correlation in abundance between Ca. Organicella extenuata and a novel ciliate of the genus Euplotes. Like Ca. Pinguicoccus supinus, we infer that Ca. Organicella extenuata is an endosymbiont of Euplotes and hypothesize that both Ca. Organicella extenuata and Ca. Pinguicocccus supinus provide fatty acids and Fe-S clusters to their Euplotes host as the foundation of a mutualistic symbiosis. The discovery of Ca. Organicella extenuata as possessing genetic code 4 illustrates that in addition to identifying endosymbionts by sequencing known symbiotic communities and searching metagenome data using reference endosymbiont genomes, the potential exists to identify novel endosymbionts by searching for unusual coding parameters. Frontiers Media S.A. 2021-06-01 /pmc/articles/PMC8204192/ /pubmed/34140946 http://dx.doi.org/10.3389/fmicb.2021.674758 Text en Copyright © 2021 Williams, Allen, Ivanova, Huntemann, Haque, Hancock, Brazendale and Cavicchioli. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Williams, Timothy J.
Allen, Michelle A.
Ivanova, Natalia
Huntemann, Marcel
Haque, Sabrina
Hancock, Alyce M.
Brazendale, Sarah
Cavicchioli, Ricardo
Genome Analysis of a Verrucomicrobial Endosymbiont With a Tiny Genome Discovered in an Antarctic Lake
title Genome Analysis of a Verrucomicrobial Endosymbiont With a Tiny Genome Discovered in an Antarctic Lake
title_full Genome Analysis of a Verrucomicrobial Endosymbiont With a Tiny Genome Discovered in an Antarctic Lake
title_fullStr Genome Analysis of a Verrucomicrobial Endosymbiont With a Tiny Genome Discovered in an Antarctic Lake
title_full_unstemmed Genome Analysis of a Verrucomicrobial Endosymbiont With a Tiny Genome Discovered in an Antarctic Lake
title_short Genome Analysis of a Verrucomicrobial Endosymbiont With a Tiny Genome Discovered in an Antarctic Lake
title_sort genome analysis of a verrucomicrobial endosymbiont with a tiny genome discovered in an antarctic lake
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8204192/
https://www.ncbi.nlm.nih.gov/pubmed/34140946
http://dx.doi.org/10.3389/fmicb.2021.674758
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