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Marine Sediments Illuminate Chlamydiae Diversity and Evolution

Dharamshi, Jennah E. ; Tamarit, Daniel ; Eme, Laura ; Stairs, Courtney W. LU orcid ; Martijn, Joran ; Homa, Felix ; Jørgensen, Steffen L. ; Spang, Anja and Ettema, Thijs J.G. (2020) In Current Biology 30(6). p.7-1048
Abstract

The bacterial phylum Chlamydiae is so far composed of obligate symbionts of eukaryotic hosts. Well known for Chlamydiaceae, pathogens of humans and other animals, Chlamydiae also include so-called environmental lineages that primarily infect microbial eukaryotes. Environmental surveys indicate that Chlamydiae are found in a wider range of environments than anticipated previously. However, the vast majority of this chlamydial diversity has been underexplored, biasing our current understanding of their biology, ecological importance, and evolution. Here, we report that previously undetected and active chlamydial lineages dominate microbial communities in deep anoxic marine sediments taken from the Arctic Mid-Ocean Ridge. Reaching relative... (More)

The bacterial phylum Chlamydiae is so far composed of obligate symbionts of eukaryotic hosts. Well known for Chlamydiaceae, pathogens of humans and other animals, Chlamydiae also include so-called environmental lineages that primarily infect microbial eukaryotes. Environmental surveys indicate that Chlamydiae are found in a wider range of environments than anticipated previously. However, the vast majority of this chlamydial diversity has been underexplored, biasing our current understanding of their biology, ecological importance, and evolution. Here, we report that previously undetected and active chlamydial lineages dominate microbial communities in deep anoxic marine sediments taken from the Arctic Mid-Ocean Ridge. Reaching relative abundances of up to 43% of the bacterial community, and a maximum diversity of 163 different species-level taxonomic units, these Chlamydiae represent important community members. Using genome-resolved metagenomics, we reconstructed 24 draft chlamydial genomes, expanding by over a third the known genomic diversity in this phylum. Phylogenomic analyses revealed several novel clades across the phylum, including a previously unknown sister lineage of the Chlamydiaceae, providing new insights into the origin of pathogenicity in this family. We were unable to identify putative eukaryotic hosts for these marine sediment chlamydiae, despite identifying genomic features that may be indicative of host-association. The high abundance and genomic diversity of Chlamydiae in these anoxic marine sediments indicate that some members could play an important, and thus far overlooked, ecological role in such environments and may indicate alternate lifestyle strategies. Dharamshi et al. find abundant, diverse, and active Chlamydiae in deep anoxic marine sediments. Using metagenomics, chlamydial genomes are obtained that form several new clades. Analyses of these genomes provide new insights into the evolution and host association of the Chlamydiae phylum, indicating that some are not symbionts of eukaryotic hosts.

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author
; ; ; ; ; ; ; and
publishing date
type
Contribution to journal
publication status
published
keywords
anoxic marine sediment, Chlamydia, metagenomics, microbe-host association, microbial community, microbial evolution, PVC superphylum, symbiosis, uncultured microbial diversity
in
Current Biology
volume
30
issue
6
pages
7 - 1048
publisher
Elsevier
external identifiers
  • scopus:85081645045
  • pmid:32142706
ISSN
0960-9822
DOI
10.1016/j.cub.2020.02.016
language
English
LU publication?
no
id
7f731358-e3a8-4040-a915-bec040473292
date added to LUP
2020-10-23 10:47:45
date last changed
2024-04-17 16:46:31
@article{7f731358-e3a8-4040-a915-bec040473292,
  abstract     = {{<p>The bacterial phylum Chlamydiae is so far composed of obligate symbionts of eukaryotic hosts. Well known for Chlamydiaceae, pathogens of humans and other animals, Chlamydiae also include so-called environmental lineages that primarily infect microbial eukaryotes. Environmental surveys indicate that Chlamydiae are found in a wider range of environments than anticipated previously. However, the vast majority of this chlamydial diversity has been underexplored, biasing our current understanding of their biology, ecological importance, and evolution. Here, we report that previously undetected and active chlamydial lineages dominate microbial communities in deep anoxic marine sediments taken from the Arctic Mid-Ocean Ridge. Reaching relative abundances of up to 43% of the bacterial community, and a maximum diversity of 163 different species-level taxonomic units, these Chlamydiae represent important community members. Using genome-resolved metagenomics, we reconstructed 24 draft chlamydial genomes, expanding by over a third the known genomic diversity in this phylum. Phylogenomic analyses revealed several novel clades across the phylum, including a previously unknown sister lineage of the Chlamydiaceae, providing new insights into the origin of pathogenicity in this family. We were unable to identify putative eukaryotic hosts for these marine sediment chlamydiae, despite identifying genomic features that may be indicative of host-association. The high abundance and genomic diversity of Chlamydiae in these anoxic marine sediments indicate that some members could play an important, and thus far overlooked, ecological role in such environments and may indicate alternate lifestyle strategies. Dharamshi et al. find abundant, diverse, and active Chlamydiae in deep anoxic marine sediments. Using metagenomics, chlamydial genomes are obtained that form several new clades. Analyses of these genomes provide new insights into the evolution and host association of the Chlamydiae phylum, indicating that some are not symbionts of eukaryotic hosts.</p>}},
  author       = {{Dharamshi, Jennah E. and Tamarit, Daniel and Eme, Laura and Stairs, Courtney W. and Martijn, Joran and Homa, Felix and Jørgensen, Steffen L. and Spang, Anja and Ettema, Thijs J.G.}},
  issn         = {{0960-9822}},
  keywords     = {{anoxic marine sediment; Chlamydia; metagenomics; microbe-host association; microbial community; microbial evolution; PVC superphylum; symbiosis; uncultured microbial diversity}},
  language     = {{eng}},
  month        = {{03}},
  number       = {{6}},
  pages        = {{7--1048}},
  publisher    = {{Elsevier}},
  series       = {{Current Biology}},
  title        = {{Marine Sediments Illuminate Chlamydiae Diversity and Evolution}},
  url          = {{http://dx.doi.org/10.1016/j.cub.2020.02.016}},
  doi          = {{10.1016/j.cub.2020.02.016}},
  volume       = {{30}},
  year         = {{2020}},
}