Sulfur-oxidizing symbionts without canonical genes for autotrophic CO2 fixation

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

Research output: Contribution to journalArticlepeer-review

24 Scopus citations

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.
Original languageEnglish (US)
JournalmBio
Volume10
Issue number3
DOIs
StatePublished - Jun 24 2019

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: We thank our fieldwork hosts: the HYDRA Institute on Elba, especially Miriam Weber, Hannah Kuhfuß, and Matthias Schneider; the Smithsonian CCRE program and staff at the Carrie Bow Caye field station; and Lasse Riemann and the Marine Biological Section, University of Copenhagen. Mario Schimak, Oliver Jäckle, Juliane Wippler, Judith Zim-mermann, Miriam Sadowski, Silke Wetzel, Nikolaus Leisch, and Anne-Christin Kreutz-mann assisted in sample collection. Library preparation and sequencing were performed at the Max Planck Genome Centre Cologne. We thank Marc Strous for access to proteomics equipment. We thank Dolma Michellod and Alexander Gruhl for collecting DIC samples and Henning Kuhnert and the MARUM Stable Isotope Labora‏tory‏ tea‏m ‏for DIC IRMS measurements. We also thank Roland Dieterich for computational support; Caitlin Petro, Erik Puskas, Tora Gulstad, and Frantisek Fojt for mass spectrometry support; and Lizbeth Sayavedra, Oliver Müller-Cajar, Monika Bright, Jörg Ott, Verena Carvalho, Cameron Callbeck, Marc Mußmann, and members of the Symbiosis Department for useful discussions and comments. The proteomics and direct protein-SIF work was supported by the Campus Alberta Innovation Chair Program, the Canadian Foundation for Innovation, and a discovery grant from the Natural Sciences and Engineering Research Council (NSERC) of Canada (above to Marc Strous) and the NC State Chancellor’s Faculty Excellence Program Cluster on Microbiomes and Complex Microbial Communities (M.K.). Financial support was provided by the Max Planck Society; the Humboldt Foundation to C.P.A.; a Marie Curie Fellowship to H.R.G.-V.; the Gordon and Betty Moore Foundation Marine Microbial Initiative Investigator Award to N.D. (grant GBMF3811); SFB 987 “Microbial Diversity in Environmental Signal Response” to L.S.V.B. and T.J.E.; and FET-Open grant 686330 (Future Agriculture) to J.Z.

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