Original Article

The ISME Journal (2016) 10, 376–388; doi:10.1038/ismej.2015.119; published online 14 July 2015

A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior

Antonia Klein1,8, Lukas Schrader1,8, Rosario Gil2, Alejandro Manzano-Marín2, Laura Flórez3, David Wheeler5, John H Werren6, Amparo Latorre2,7, Jürgen Heinze1, Martin Kaltenpoth3,4, Andrés Moya2 and Jan Oettler1

  1. 1Institut für Zoologie, Universität Regensburg, Regensburg, Germany
  2. 2Institut Canvanilles de Biodiversitat i Biologia Evolutiva (ICBiBE), Parc Cientific de la Universitat de Valencia, Paterna (Valencia), Spain
  3. 3Max Planck Institute for Chemical Ecology, Jena, Germany
  4. 4Johannes Gutenberg University Mainz, Institute for Zoology, Department for Evolutionary Ecology, Mainz, Germany
  5. 5Institute of Fundamental Sciences, Massey University, Palmerston North, New Zealand
  6. 6Department of Biology, University Rochester, Rochester, NY, USA
  7. 7Área de Genómica y Salud de la Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana (FISABIO)–Salud Pública, Valencia, Spain

Correspondence: J Oettler, Institut für Zoologie, Universität Regensburg, Universitätsstrasse 31, Regensburg 93053, Germany. E-mail: joettler@gmail.com

8These authors contributed equally to this work.

Received 9 January 2015; Revised 29 April 2015; Accepted 9 June 2015
Advance online publication 14 July 2015

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Abstract

The evolution of eukaryotic organisms is often strongly influenced by microbial symbionts that confer novel traits to their hosts. Here we describe the intracellular Enterobacteriaceae symbiont of the invasive ant Cardiocondyla obscurior, ‘Candidatus Westeberhardia cardiocondylae’. Upon metamorphosis, Westeberhardia is found in gut-associated bacteriomes that deteriorate following eclosion. Only queens maintain Westeberhardia in the ovarian nurse cells from where the symbionts are transmitted to late-stage oocytes during nurse cell depletion. Functional analyses of the streamlined genome of Westeberhardia (533kb, 23.41% GC content) indicate that neither vitamins nor essential amino acids are provided for the host. However, the genome encodes for an almost complete shikimate pathway leading to 4-hydroxyphenylpyruvate, which could be converted into tyrosine by the host. Taken together with increasing titers of Westeberhardia during pupal stage, this suggests a contribution of Westeberhardia to cuticle formation. Despite a widespread occurrence of Westeberhardia across host populations, one ant lineage was found to be naturally symbiont-free, pointing to the loss of an otherwise prevalent endosymbiont. This study yields insights into a novel intracellular mutualist that could play a role in the invasive success of C. obscurior.