Conservation of the glycogen metabolism pathway underlines a pivotal function of storage polysaccharides in Chlamydiae

Colpaert, Matthieu; Kadouche, Derifa; Ducatez, Mathieu; Pillonel, Trestan; Kebbi-Beghdadi, Carole; Cenci, Ugo; Huang, Bin; Chabi, Malika; Maës, Emmanuel; Coddeville, Bernadette; Couderc, Loïc; Touzet, Hélène; Bray, Fabrice; Tirtiaux, Catherine; Ball, Steven; Greub, Gilbert; Colleoni, Christophe

doi:10.1038/s42003-021-01794-y

Cited by 18 publications

(23 citation statements)

References 71 publications

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“…This includes almost all of the genes constituting the chlamydial core genome [ 18 , 24 ], such as the type III secretion system [ 44 ], nucleotide transport proteins (Ntt1/Ntt2) [ 45 ], the master regulator of the chlamydial developmental cycle (Euo) [ 46 ] as well as major effector proteins (CopN, Pkn5) [ 47 , 48 ] that interfere with host cellular pathways. Further, glycogen metabolism is conserved among all Rhabdochlamydiaceae , this is consistent with the importance of glycogen as storage compound for many known chlamydiae [ 49 ].…”

Section: Resultssupporting

confidence: 66%

Ecology and evolution of chlamydial symbionts of arthropods

Halter

Köstlbacher²,

Collingro³

et al. 2022

ISME Communications

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The phylum Chlamydiae consists of obligate intracellular bacteria including major human pathogens and diverse environmental representatives. Here we investigated the Rhabdochlamydiaceae, which is predicted to be the largest and most diverse chlamydial family, with the few described members known to infect arthropod hosts. Using published 16 S rRNA gene sequence data we identified at least 388 genus-level lineages containing about 14 051 putative species within this family. We show that rhabdochlamydiae are mainly found in freshwater and soil environments, suggesting the existence of diverse, yet unknown hosts. Next, we used a comprehensive genome dataset including metagenome assembled genomes classified as members of the family Rhabdochlamydiaceae, and we added novel complete genome sequences of Rhabdochlamydia porcellionis infecting the woodlouse Porcellio scaber, and of ‘Candidatus R. oedothoracis’ associated with the linyphiid dwarf spider Oedothorax gibbosus. Comparative analysis of basic genome features and gene content with reference genomes of well-studied chlamydial families with known host ranges, namely Parachlamydiaceae (protist hosts) and Chlamydiaceae (human and other vertebrate hosts) suggested distinct niches for members of the Rhabdochlamydiaceae. We propose that members of the family represent intermediate stages of adaptation of chlamydiae from protists to vertebrate hosts. Within the genus Rhabdochlamydia, pronounced genome size reduction could be observed (1.49–1.93 Mb). The abundance and genomic distribution of transposases suggests transposable element expansion and subsequent gene inactivation as a mechanism of genome streamlining during adaptation to new hosts. This type of genome reduction has never been described before for any member of the phylum Chlamydiae. This study provides new insights into the molecular ecology, genomic diversity, and evolution of representatives of one of the most divergent chlamydial families.

show abstract

Section: Resultssupporting

confidence: 66%

Ecology and evolution of chlamydial symbionts of arthropods

Halter

Köstlbacher²,

Collingro³

et al. 2022

ISME Communications

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show abstract

“…Further, glycogen metabolism is conserved among all Rhabdochlamydiaceae, this is consistent with the importance of glycogen as storage compound for many known chlamydiae [49].…”

Section: The Rhabdochlamydiaceae Pangenomesupporting

confidence: 79%

Ecology and evolution of chlamydial symbionts of arthropods

Halter

Köstlbacher

Collingro

et al. 2022

Preprint

View full text Add to dashboard Cite

The phylum Chlamydiae consists of obligate intracellular bacteria including major human pathogens and diverse environmental representatives. Here we investigated the Rhabdochlamydiaceae, which is predicted to be the largest and most diverse chlamydial family, with the few described members known to infect arthropod hosts. Using published 16S rRNA gene sequence data we identified at least 388 genus-level lineages containing about 14 051 putative species within this family. We show that rhabdochlamydiae are mainly found in freshwater and soil environments, suggesting the existence of diverse, yet unknown hosts. Next, we used a comprehensive genome dataset including metagenome assembled genomes classified as members of the family Rhabdochlamydiaceae, and we added novel complete genome sequences of Rhabdochlamydia porcellionis infecting the woodlouse Porcellio scaber, and of 'Candidatus R. oedothoracis' associated with the linyphiid dwarf spider Oedothorax gibbosus. Comparative analysis of basic genome features and gene content with reference genomes of well-studied chlamydial families with known host ranges, namely Parachlamydiaceae (protist hosts) and Chlamydiaceae (human and other vertebrate hosts) suggested distinct niches for members of the Rhabdochlamydiaceae. We propose that members of the family represent intermediate stages of adaptation of chlamydiae from protists to vertebrate hosts. Within the genus Rhabdochlamydia, pronounced genome size reduction could be observed (1.49-1.93 Mb). The abundance and genomic distribution of transposases suggests transposable element expansion and subsequent gene inactivation as a mechanism of genome streamlining during adaptation to new hosts. This type of genome reduction has never been described before for any member of the phylum Chlamydiae. This study provides new insights into the molecular ecology, genomic diversity, and evolution of representatives of one of the most divergent chlamydial families.

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“…In line with the hypothesis that metabolism is a key determinant of elementary body infectivity (42,61), it is possible that elementary bodies only marginally rely on external supplies of nutrients and use their own store of glycogen. Glycogen particles were indeed observed in elementary bodies and enzymes necessary for its synthesis are well conserved in the Chlamydiales order (63). Incubating elementary bodies at higher temperatures could therefore induce a faster metabolic rate and deplete the glycogen stores of elementary bodies.…”

Section: Discussionmentioning

confidence: 99%

Temperature affects the host range of Rhabdochlamydia porcellionis and the infectivity of Waddlia chondrophila and Chlamydia trachomatis elementary bodies

Marquis

Ardissone

Greub

2022

Preprint

Self Cite

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The Rhabdochlamydiaceae family is a recent addition to the Chlamydiales order. Its members were discovered in cockroaches and woodlice but recent metagenomics surveys demonstrated the widespread distribution of this family in the environment. It was moreover estimated to be the largest family of the Chlamydiales order based on 16S rRNA encoding gene diversity. Unlike most chlamydia-like organisms, no Rhabdochlamydiaceae could be co-cultivated in amoebae and its host range remains largely unknown. Here, we tested the permissivity of various mammalian and arthropod cell lines to determine the host range of Rhabdochlamydia porcellionis, the only cultured representative of this family. While a growth could initially only be obtained in the Sf9 cell line, lowering the incubation temperature of the mammalian cells from 37 °C to 28 °C allowed R. porcellionis to grow in those cells. Furthermore, a 6 h exposure to 37 °C was sufficient to irreversibly block the replication of R. porcellionis, suggesting that this bacterium either lost or never acquired the ability to grow at 37 °C. We next sought to determine if temperature would also affect the infectivity of elementary bodies. Although we could not purify enough bacteria to reach a conclusive result for R. porcellionis, our experiment showed that the elementary bodies of Chlamydia trachomatis and Waddlia chondrophila lose their infectivity faster at 37 °C than at room temperature. Our results demonstrate that members of the Chlamydiales adapt to the temperature of their host organism and that this adaptation can in turn restrict their host range.

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Conservation of the glycogen metabolism pathway underlines a pivotal function of storage polysaccharides in Chlamydiae

Cited by 18 publications

References 71 publications

Ecology and evolution of chlamydial symbionts of arthropods

Ecology and evolution of chlamydial symbionts of arthropods

Ecology and evolution of chlamydial symbionts of arthropods

Temperature affects the host range of Rhabdochlamydia porcellionis and the infectivity of Waddlia chondrophila and Chlamydia trachomatis elementary bodies

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