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

doi:10.3389/fmicb.2021.674758

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

Journal Article · Tue Jun 01 00:00:00 EDT 2021 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2021.674758· OSTI ID:1904150

Williams, Timothy J. ^[1]; Allen, Michelle A. ^[1]; Ivanova, Natalia ^[2]; Huntemann, Marcel ^[2]; Haque, Sabrina ^[1]; Hancock, Alyce M. ^[3]; Brazendale, Sarah ^[4]; Cavicchioli, Ricardo ^[1]

Univ. of New South Wales, Sydney, NSW (Australia)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Univ. of New South Wales, Sydney, NSW (Australia); Univ. of Tasmania, Battery Point, TAS (Australia)
Univ. of New South Wales, Sydney, NSW (Australia); King Island Brewhouse, Pegarah, TAS (Australia)

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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Research Organization:: USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); Australian Research Council (ARC)

Grant/Contract Number:: AC02-05CH11231; DP150100244

OSTI ID:: 1904150

Journal Information:: Frontiers in Microbiology, Vol. 12; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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