Biphasic Metabolism and Host Interaction of a Chlamydial Symbiont

ABSTRACT Chlamydiae are obligate intracellular bacteria comprising well-known human pathogens and ubiquitous symbionts of protists, which are characterized by a unique developmental cycle. Here we comprehensively analyzed gene expression dynamics of Protochlamydia amoebophila during infection of its...

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Autores principales:	Lena König, Alexander Siegl, Thomas Penz, Susanne Haider, Cecilia Wentrup, Julia Polzin, Evelyne Mann, Stephan Schmitz-Esser, Daryl Domman, Matthias Horn
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Protochlamydia RNA-seq chlamydia developmental cycle gene expression host-microbe interaction Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/906b3cb8ac4b45da8757cb8bde444f01
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spelling	oai:doaj.org-article:906b3cb8ac4b45da8757cb8bde444f012021-12-02T19:45:29ZBiphasic Metabolism and Host Interaction of a Chlamydial Symbiont10.1128/mSystems.00202-162379-5077https://doaj.org/article/906b3cb8ac4b45da8757cb8bde444f012017-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00202-16https://doaj.org/toc/2379-5077ABSTRACT Chlamydiae are obligate intracellular bacteria comprising well-known human pathogens and ubiquitous symbionts of protists, which are characterized by a unique developmental cycle. Here we comprehensively analyzed gene expression dynamics of Protochlamydia amoebophila during infection of its Acanthamoeba host by RNA sequencing. This revealed a highly dynamic transcriptional landscape, where major transcriptional shifts are conserved among chlamydial symbionts and pathogens. Our data served to propose a time-resolved model for type III protein secretion during the developmental cycle, and we provide evidence for a biphasic metabolism of P. amoebophila during infection, which involves energy parasitism and amino acids as the carbon source during initial stages and a postreplicative switch to endogenous glucose-based ATP production. This fits well with major transcriptional changes in the amoeba host, where upregulation of complex sugar breakdown precedes the P. amoebophila metabolic switch. The biphasic chlamydial metabolism represents a unique adaptation to exploit eukaryotic host cells, which likely contributed to the evolutionary success of this group of microbes. IMPORTANCE Chlamydiae are known as major bacterial pathogens of humans, causing the ancient disease trachoma, but they are also frequently found in the environment where they infect ubiquitous protists such as amoebae. All known chlamydiae require a eukaryotic host cell to thrive. Using the environmental chlamydia Protochlamydia amoebophila within its natural host, Acanthamoeba castellanii, we investigated gene expression dynamics in vivo and throughout the complete chlamydial developmental cycle for the first time. This allowed us to infer how a major virulence mechanism, the type III secretion system, is regulated and employed, and we show that the physiology of chlamydiae undergoes a complete shift regarding carbon metabolism and energy generation. This study provides comprehensive insights into the infection strategy of chlamydiae and reveals a unique adaptation to life within a eukaryotic host cell.Lena KönigAlexander SieglThomas PenzSusanne HaiderCecilia WentrupJulia PolzinEvelyne MannStephan Schmitz-EsserDaryl DommanMatthias HornAmerican Society for MicrobiologyarticleProtochlamydiaRNA-seqchlamydiadevelopmental cyclegene expressionhost-microbe interactionMicrobiologyQR1-502ENmSystems, Vol 2, Iss 3 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Protochlamydia RNA-seq chlamydia developmental cycle gene expression host-microbe interaction Microbiology QR1-502
spellingShingle	Protochlamydia RNA-seq chlamydia developmental cycle gene expression host-microbe interaction Microbiology QR1-502 Lena König Alexander Siegl Thomas Penz Susanne Haider Cecilia Wentrup Julia Polzin Evelyne Mann Stephan Schmitz-Esser Daryl Domman Matthias Horn Biphasic Metabolism and Host Interaction of a Chlamydial Symbiont
description	ABSTRACT Chlamydiae are obligate intracellular bacteria comprising well-known human pathogens and ubiquitous symbionts of protists, which are characterized by a unique developmental cycle. Here we comprehensively analyzed gene expression dynamics of Protochlamydia amoebophila during infection of its Acanthamoeba host by RNA sequencing. This revealed a highly dynamic transcriptional landscape, where major transcriptional shifts are conserved among chlamydial symbionts and pathogens. Our data served to propose a time-resolved model for type III protein secretion during the developmental cycle, and we provide evidence for a biphasic metabolism of P. amoebophila during infection, which involves energy parasitism and amino acids as the carbon source during initial stages and a postreplicative switch to endogenous glucose-based ATP production. This fits well with major transcriptional changes in the amoeba host, where upregulation of complex sugar breakdown precedes the P. amoebophila metabolic switch. The biphasic chlamydial metabolism represents a unique adaptation to exploit eukaryotic host cells, which likely contributed to the evolutionary success of this group of microbes. IMPORTANCE Chlamydiae are known as major bacterial pathogens of humans, causing the ancient disease trachoma, but they are also frequently found in the environment where they infect ubiquitous protists such as amoebae. All known chlamydiae require a eukaryotic host cell to thrive. Using the environmental chlamydia Protochlamydia amoebophila within its natural host, Acanthamoeba castellanii, we investigated gene expression dynamics in vivo and throughout the complete chlamydial developmental cycle for the first time. This allowed us to infer how a major virulence mechanism, the type III secretion system, is regulated and employed, and we show that the physiology of chlamydiae undergoes a complete shift regarding carbon metabolism and energy generation. This study provides comprehensive insights into the infection strategy of chlamydiae and reveals a unique adaptation to life within a eukaryotic host cell.
format	article
author	Lena König Alexander Siegl Thomas Penz Susanne Haider Cecilia Wentrup Julia Polzin Evelyne Mann Stephan Schmitz-Esser Daryl Domman Matthias Horn
author_facet	Lena König Alexander Siegl Thomas Penz Susanne Haider Cecilia Wentrup Julia Polzin Evelyne Mann Stephan Schmitz-Esser Daryl Domman Matthias Horn
author_sort	Lena König
title	Biphasic Metabolism and Host Interaction of a Chlamydial Symbiont
title_short	Biphasic Metabolism and Host Interaction of a Chlamydial Symbiont
title_full	Biphasic Metabolism and Host Interaction of a Chlamydial Symbiont
title_fullStr	Biphasic Metabolism and Host Interaction of a Chlamydial Symbiont
title_full_unstemmed	Biphasic Metabolism and Host Interaction of a Chlamydial Symbiont
title_sort	biphasic metabolism and host interaction of a chlamydial symbiont
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/906b3cb8ac4b45da8757cb8bde444f01
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Biphasic Metabolism and Host Interaction of a Chlamydial Symbiont

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