Chlamydiae as symbionts of photosynthetic dinoflagellates

Author(s)
Justin Maire, Astrid Collingro, Kshitij Tandon, The Parkville, Louise M Judd, Matthias Horn, Linda L Blackall, Madeleine J H van Oppen
Abstract

Chlamydiae are ubiquitous intracellular bacteria and infect a wide diversity of eukaryotes, including mammals. However, chlamydiae have never been reported to infect photosynthetic organisms. Here, we describe a novel chlamydial genus and species, Candidatus Algichlamydia australiensis, capable of infecting the photosynthetic dinoflagellate Cladocopium sp. (originally isolated from a scleractinian coral). Algichlamydia australiensis was confirmed to be intracellular by fluorescence in situ hybridization and confocal laser scanning microscopy and temporally stable at the population level by monitoring its relative abundance across four weeks of host growth. Using a combination of short- and long-read sequencing, we recovered a high-quality (completeness 91.73% and contamination 0.27%) metagenome-assembled genome of A. australiensis. Phylogenetic analyses show that this chlamydial taxon represents a new genus and species within the Simkaniaceae family. Algichlamydia australiensis possesses all the hallmark genes for chlamydiae-host interactions, including a complete type III secretion system. In addition, a type IV secretion system is encoded on a plasmid and has previously been observed for only three other chlamydial species. Twenty orthologous groups of genes are unique to A. australiensis, one of which is structurally similar to a protein known from Cyanobacteria and Archaeplastida involved in thylakoid biogenesis and maintenance, hinting at potential chlamydiae interactions with the chloroplasts of Cladocopium cells. Our study shows that chlamydiae infect dinoflagellate symbionts of cnidarians, the first photosynthetic organism reported to harbor chlamydiae, thereby expanding the breadth of chlamydial hosts and providing a new contribution to the discussion around the role of chlamydiae in the establishment of the primary plastid.

Organisation(s)
Department of Microbiology and Ecosystem Science
External organisation(s)
University of Melbourne, Australian Institute of Marine Science, The Peter Doherty Institute for Infection and Immunity
Journal
The ISME Journal
Volume
18
No. of pages
15
ISSN
1751-7362
DOI
https://doi.org/10.1093/ismejo/wrae139
Publication date
01-2024
Peer reviewed
Yes
Austrian Fields of Science 2012
106014 Genomics, 106022 Microbiology, 106021 Marine biology
Keywords
ASJC Scopus subject areas
Ecology, Evolution, Behavior and Systematics, Microbiology
Portal url
https://ucrisportal.univie.ac.at/en/publications/chlamydiae-as-symbionts-of-photosynthetic-dinoflagellates(cc6ed5d1-056d-4ad2-a3bb-41884c9ce8ea).html