Marine Sediments Illuminate Chlamydiae Diversity and Evolution

Dharamshi, Jennah E.; Tamarit, Daniel; Eme, Laura; Stairs, Courtney W.; Martijn, Joran; Homa, Félix; Jørgensen, Steffen Leth; Spang, Anja; Ettema, Thijs J. G.

doi:10.1016/j.cub.2020.02.016

Cited by 59 publications

(75 citation statements)

References 166 publications

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“…While gene order breaks down for some Alpha- and Epsilon-proteobacterial systems, as noted by Liu & Ochman (2007), it is otherwise conserved across proteobacteria as well as deep splits in the bacterial tree, including Chloroflexi, Spirochetes, Firmicutes, Nitrospirae, Thermotogae, and Verrucomicrobia. The gene order is also found in the presumed “flagellar remnant” (Betts-Hampikian and Fields 2010) system found in Chlamydiae in addition to their classic NF-T3SS; some marine Chlamydiae are now known to have flagella (Collingro et al 2017; Dharamshi et al 2020).…”

Section: Resultsmentioning

confidence: 99%

Homology between the flagellar export apparatus and ATP synthetase: evidence from synteny predating the Last Universal Common Ancestor

Matzke

Lin

Stone

et al. 2021

Preprint

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Evidence of homology between proteins in the ATP synthetase and the bacterial flagellar motor (BFM) has been accumulating since the 1980s. Specifically, the BFM’s Type 3 Secretion System (T3SS) export apparatus FliH, FliI, and FliJ are considered homologous to FO-b + F1-δ, F1-α/β, and F1-γ, and have similar structure and interactions. We review the discoveries that advanced the homology hypothesis and then conduct a further test by examining gene order in the two systems and their relatives. Conservation of gene order, or synteny, is often observed between closely related prokaryote species, but usually degrades with phylogenetic distance. As a result, observed conservation of synteny over vast phylogenetic distances can be evidence of shared ancestral coexpression, interaction, and function. We constructed a gene order dataset by examining the order of fliH, fliI, and fliJ genes across the phylogenetic breadth of flagellar and nonflagellar T3SS. We compared this to published surveys of gene order in the F1FO-ATP synthetase, its N-ATPase relatives, and the bacterial/archaeal V- and A-type ATPases. Strikingly, the fliHIJ gene order was deeply conserved, with the few exceptions appearing derived, and exactly matching the widely conserved F-ATPase gene order atpFHAG, coding for subunits b-δ-α-γ. The V/A-type ATPases have a similar conserved gene order shared for homologous components. Our results further strengthen the argument for homology between these systems, and suggest a rare case of synteny conserved over billions of years, dating back to well before the Last Universal Common Ancestor (LUCA).

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Section: Resultsmentioning

confidence: 99%

Homology between the flagellar export apparatus and ATP synthetase: evidence from synteny predating the Last Universal Common Ancestor

Matzke

Lin

Stone

et al. 2021

Preprint

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“…2c). There are currently 6 formally named and 8 proposed Chlamydiae families (Pillonel et al, 2018; Taylor-Brown et al, 2015), and several other recently discovered novel clades from marine sediments (Dharamshi et al, 2020). The D. discoideum Chlamydiae endosymbionts do not appear to be closely related (<97% sequence match) to any of these groups.…”

Section: Resultsmentioning

confidence: 99%

“…Haplotypes 6, 7 and 8 fall in different places in the phylogeny and do not group closely with any other taxa, although these haplotypes are based on only 220bp of sequence information so their taxonomic identity is less clear. Finally, while the newly discovered marine Chlamydiae lineages (Dharamshi et al, 2020) were not included in this phylogeny, when we aligned our Chlamydiae haplotypes with these sequences, the closest match had only an 89% sequence identity.…”

Section: Resultsmentioning

confidence: 99%

Novel Chlamydiae andAmoebophilusendosymbionts are prevalent in wild isolates of the model social amoebaDictyostelium discoideum

Haselkorn

Jimenez

Bashir

et al. 2020

Preprint

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Amoebae interact with bacteria in diverse and multifaceted ways. Amoeba predation can serve as a selective pressure for the development of bacterial virulence traits. Bacteria may also adapt to life inside amoebae, resulting in symbiotic relationships (pathogenic or mutualistic). Indeed, amoebae are often infected with bacterial endosymbionts. Acanthamoeba and Hartmannella harbor symbionts from five distinct lineages within the Proteobacteria, Bacteroidetes, and Chlamydiae. Here, we PCR-screened an extensive collection of Dictyostelium discoideum wild isolates for the presence of bacterial symbionts. For the first time we found that obligate symbionts are surprisingly common in this highly-studied amoeba species, identified in 42% of screened isolates (N=730). Members of the environmental Chlamydiae are particularly prevalent. These strains are novel and phylogenetically distinct. We also found Amoebophilus symbionts in 8% of screened isolates (N=730). Under laboratory conditions, antibiotic-cured amoebae behave similarly to their endosymbiont-infected counterparts, suggesting that endosymbionts do not significantly impact host fitness, at least in the laboratory. We found several natural isolates were co-infected with different endosymbionts. The high prevalence and novelty of amoeba endosymbiont clades in the model organism D. discoideum opens the door to future research on the significance and mechanisms of amoeba-symbiont interactions.

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“…For example, within the Chlamydiaceae family there are lineages that have evolved intracellular associations with eukaryotes (77,78). Recent metagenomic studies uncovered that extensive metabolic capabilities were present in the common ancestor of environmental Chlamydiia (class) and subsequently lost in Chlamydiaceae (79). Moreover, host-associated bacterial genomes show a variation in size depending on the type of host (plant, animal, etc.)…”

Section: Environmental Impact On Genome Size In Different Taxonomic Lmentioning

confidence: 99%

A genomic perspective across Earth’s microbiomes reveals that genome size in Archaea and Bacteria is linked to ecosystem type and trophic strategy

Rodríguez-Gijón

Nuy

Mehrshad

et al. 2021

Preprint

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Our view of genome size distribution in Bacteria and Archaea has remained skewed as the data used to paint its picture has been dominated by genomes of microorganisms that can be cultivated under laboratory settings. However, the continuous effort to catalogue the genetic make-up of Earth’s microbiomes, specifically propelled by recent extensive work on uncultivated microorganisms, provides a unique opportunity to revise our perspective on genome size distribution. Genome size is largely a function of the expansion and contraction, by gain or loss of DNA elements. While genome expansion provides microorganisms the capability to acquire a wide repertoire of ecological functions, genome reduction increases the fitness of the microorganisms to very specific niches. Capitalizing on a recently released large catalog of tens of thousands of metagenome-assembled genomes, we here provide a comprehensive overview of genome size distributions, suggesting that the known phylogenetic diversity of environmental microorganisms possess significantly smaller genomes (aquatic bacteria average 3.1 Mb, host-associated bacterial genomes average 3.0 Mb, and terrestrial bacteria average 3.8 Mb) than the collection of laboratory isolated microorganisms (average 4.4 Mb). Moreover, the variation in genome sizes across different types of environments reflects the different ecological and evolutionary strategies used by microorganisms to thrive in their native environment. Finally, the fact that genome sizes in Bacteria and Archaea remain relatively small might be a reflection of the constraints imposed by selection and an overall dominance of gene loss as a survival strategy.

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Marine Sediments Illuminate Chlamydiae Diversity and Evolution

Cited by 59 publications

References 166 publications

Homology between the flagellar export apparatus and ATP synthetase: evidence from synteny predating the Last Universal Common Ancestor

Homology between the flagellar export apparatus and ATP synthetase: evidence from synteny predating the Last Universal Common Ancestor

Novel Chlamydiae andAmoebophilusendosymbionts are prevalent in wild isolates of the model social amoebaDictyostelium discoideum

A genomic perspective across Earth’s microbiomes reveals that genome size in Archaea and Bacteria is linked to ecosystem type and trophic strategy

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