Sulfur-Oxidizing Symbionts without Canonical Genes for Autotrophic CO<sub>2</sub> Fixation

ABSTRACT Since the discovery of symbioses between sulfur-oxidizing (thiotrophic) bacteria and invertebrates at hydrothermal vents over 40 years ago, it has been assumed that autotrophic fixation of CO2 by the symbionts drives these nutritional associations. In this study, we investigated “Candidatus...

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Autores principales:	Brandon K. B. Seah, Chakkiath Paul Antony, Bruno Huettel, Jan Zarzycki, Lennart Schada von Borzyskowski, Tobias J. Erb, Angela Kouris, Manuel Kleiner, Manuel Liebeke, Nicole Dubilier, Harald R. Gruber-Vodicka
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	gammaproteobacteria chemosynthesis ectosymbiont lithoheterotrophy meiofauna protist Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8c010c002eb844cdaf9ed0fd2ce78cd1
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spelling	oai:doaj.org-article:8c010c002eb844cdaf9ed0fd2ce78cd12021-11-15T15:55:24ZSulfur-Oxidizing Symbionts without Canonical Genes for Autotrophic CO<sub>2</sub> Fixation10.1128/mBio.01112-192150-7511https://doaj.org/article/8c010c002eb844cdaf9ed0fd2ce78cd12019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01112-19https://doaj.org/toc/2150-7511ABSTRACT Since the discovery of symbioses between sulfur-oxidizing (thiotrophic) bacteria and invertebrates at hydrothermal vents over 40 years ago, it has been assumed that autotrophic fixation of CO2 by the symbionts drives these nutritional associations. In this study, we investigated “Candidatus Kentron,” the clade of symbionts hosted by Kentrophoros, a diverse genus of ciliates which are found in marine coastal sediments around the world. Despite being the main food source for their hosts, Kentron bacteria lack the key canonical genes for any of the known pathways for autotrophic carbon fixation and have a carbon stable isotope fingerprint that is unlike other thiotrophic symbionts from similar habitats. Our genomic and transcriptomic analyses instead found metabolic features consistent with growth on organic carbon, especially organic and amino acids, for which they have abundant uptake transporters. All known thiotrophic symbionts have converged on using reduced sulfur to gain energy lithotrophically, but they are diverse in their carbon sources. Some clades are obligate autotrophs, while many are mixotrophs that can supplement autotrophic carbon fixation with heterotrophic capabilities similar to those in Kentron. Here we show that Kentron bacteria are the only thiotrophic symbionts that appear to be entirely heterotrophic, unlike all other thiotrophic symbionts studied to date, which possess either the Calvin-Benson-Bassham or the reverse tricarboxylic acid cycle for autotrophy. IMPORTANCE Many animals and protists depend on symbiotic sulfur-oxidizing bacteria as their main food source. These bacteria use energy from oxidizing inorganic sulfur compounds to make biomass autotrophically from CO2, serving as primary producers for their hosts. Here we describe a clade of nonautotrophic sulfur-oxidizing symbionts, “Candidatus Kentron,” associated with marine ciliates. They lack genes for known autotrophic pathways and have a carbon stable isotope fingerprint heavier than other symbionts from similar habitats. Instead, they have the potential to oxidize sulfur to fuel the uptake of organic compounds for heterotrophic growth, a metabolic mode called chemolithoheterotrophy that is not found in other symbioses. Although several symbionts have heterotrophic features to supplement primary production, in Kentron they appear to supplant it entirely.Brandon K. B. SeahChakkiath Paul AntonyBruno HuettelJan ZarzyckiLennart Schada von BorzyskowskiTobias J. ErbAngela KourisManuel KleinerManuel LiebekeNicole DubilierHarald R. Gruber-VodickaAmerican Society for MicrobiologyarticlegammaproteobacteriachemosynthesisectosymbiontlithoheterotrophymeiofaunaprotistMicrobiologyQR1-502ENmBio, Vol 10, Iss 3 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	gammaproteobacteria chemosynthesis ectosymbiont lithoheterotrophy meiofauna protist Microbiology QR1-502
spellingShingle	gammaproteobacteria chemosynthesis ectosymbiont lithoheterotrophy meiofauna protist Microbiology QR1-502 Brandon K. B. Seah Chakkiath Paul Antony Bruno Huettel Jan Zarzycki Lennart Schada von Borzyskowski Tobias J. Erb Angela Kouris Manuel Kleiner Manuel Liebeke Nicole Dubilier Harald R. Gruber-Vodicka Sulfur-Oxidizing Symbionts without Canonical Genes for Autotrophic CO<sub>2</sub> Fixation
description	ABSTRACT Since the discovery of symbioses between sulfur-oxidizing (thiotrophic) bacteria and invertebrates at hydrothermal vents over 40 years ago, it has been assumed that autotrophic fixation of CO2 by the symbionts drives these nutritional associations. In this study, we investigated “Candidatus Kentron,” the clade of symbionts hosted by Kentrophoros, a diverse genus of ciliates which are found in marine coastal sediments around the world. Despite being the main food source for their hosts, Kentron bacteria lack the key canonical genes for any of the known pathways for autotrophic carbon fixation and have a carbon stable isotope fingerprint that is unlike other thiotrophic symbionts from similar habitats. Our genomic and transcriptomic analyses instead found metabolic features consistent with growth on organic carbon, especially organic and amino acids, for which they have abundant uptake transporters. All known thiotrophic symbionts have converged on using reduced sulfur to gain energy lithotrophically, but they are diverse in their carbon sources. Some clades are obligate autotrophs, while many are mixotrophs that can supplement autotrophic carbon fixation with heterotrophic capabilities similar to those in Kentron. Here we show that Kentron bacteria are the only thiotrophic symbionts that appear to be entirely heterotrophic, unlike all other thiotrophic symbionts studied to date, which possess either the Calvin-Benson-Bassham or the reverse tricarboxylic acid cycle for autotrophy. IMPORTANCE Many animals and protists depend on symbiotic sulfur-oxidizing bacteria as their main food source. These bacteria use energy from oxidizing inorganic sulfur compounds to make biomass autotrophically from CO2, serving as primary producers for their hosts. Here we describe a clade of nonautotrophic sulfur-oxidizing symbionts, “Candidatus Kentron,” associated with marine ciliates. They lack genes for known autotrophic pathways and have a carbon stable isotope fingerprint heavier than other symbionts from similar habitats. Instead, they have the potential to oxidize sulfur to fuel the uptake of organic compounds for heterotrophic growth, a metabolic mode called chemolithoheterotrophy that is not found in other symbioses. Although several symbionts have heterotrophic features to supplement primary production, in Kentron they appear to supplant it entirely.
format	article
author	Brandon K. B. Seah Chakkiath Paul Antony Bruno Huettel Jan Zarzycki Lennart Schada von Borzyskowski Tobias J. Erb Angela Kouris Manuel Kleiner Manuel Liebeke Nicole Dubilier Harald R. Gruber-Vodicka
author_facet	Brandon K. B. Seah Chakkiath Paul Antony Bruno Huettel Jan Zarzycki Lennart Schada von Borzyskowski Tobias J. Erb Angela Kouris Manuel Kleiner Manuel Liebeke Nicole Dubilier Harald R. Gruber-Vodicka
author_sort	Brandon K. B. Seah
title	Sulfur-Oxidizing Symbionts without Canonical Genes for Autotrophic CO<sub>2</sub> Fixation
title_short	Sulfur-Oxidizing Symbionts without Canonical Genes for Autotrophic CO<sub>2</sub> Fixation
title_full	Sulfur-Oxidizing Symbionts without Canonical Genes for Autotrophic CO<sub>2</sub> Fixation
title_fullStr	Sulfur-Oxidizing Symbionts without Canonical Genes for Autotrophic CO<sub>2</sub> Fixation
title_full_unstemmed	Sulfur-Oxidizing Symbionts without Canonical Genes for Autotrophic CO<sub>2</sub> Fixation
title_sort	sulfur-oxidizing symbionts without canonical genes for autotrophic co<sub>2</sub> fixation
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/8c010c002eb844cdaf9ed0fd2ce78cd1
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Sulfur-Oxidizing Symbionts without Canonical Genes for Autotrophic CO<sub>2</sub> Fixation

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