Abstract
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.
Highlights
Bacteria with highly reduced genome sizes are only found as hostrestricted symbionts and pathogens (Supplementary Table 1; Moran and Bennett, 2014)
During analyses of unusual coding parameters in metagenome contigs, we discovered a 158kbp verrucomicrobial metagenome assembled genome (MAG) that was assembled from new metagenome data derived from a complete seasonal cycle of Organic Lake
The highly restricted genomic potential illustrates this bacterium would not be capable of autonomous growth, and we name it Candidatus Organicella extenuata gen. et. sp. nov.; the genus name derives from the locality from where the MAG sequence was originally recovered (Organic Lake, Antarctica) with the addition of the diminutive Latin suffix -ella; the species “extenuata” means reduced or diminished in Latin and is in reference to the highly reduced genome
Summary
Bacteria with highly reduced genome sizes are only found as hostrestricted symbionts and pathogens (Supplementary Table 1; Moran and Bennett, 2014). Some verrucomicrobia have entered into very close symbiotic associations with eukaryotic hosts, including anti-predator ectosymbionts (epixenosomes) of the ciliate Euplotidium (Petroni et al, 2000) and various endosymbionts, such as inside the cytoplasm of intestinal and ovarial cells of nematode worms (Vandekerckhove et al, 2002), nuclei of cellulolytic protists (Sato et al, 2014), and the cytoplasm of the ciliate Euplotes vanleeuwenhoeki (Serra et al, 2020). Candidatus Xiphinematobacter, the verrucomicrobial endosymbiont of nematodes, has a 0.916-Mbp metagenome assembled genome (MAG) encoding 817 predicted proteincoding sequences (CDS); compared with free-living relatives, genes are retained for the biosynthesis of amino acids predicted to be required by their nematode hosts (Brown et al, 2015). Pinguicoccus supinus has an ‘extremely reduced genome’ at only 0.163 Mbp and encodes 168 CDS (Serra et al, 2020)
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
