Environmental Breviatea harbour mutualistic Arcobacter epibionts

• Published in: Nature (London) 2016-06, Vol.534 (7606), p.254-258
• Main Authors: Hamann, Emmo, Gruber-Vodicka, Harald, Kleiner, Manuel, Tegetmeyer, Halina E., Riedel, Dietmar, Littmann, Sten, Chen, Jianwei, Milucka, Jana, Viehweger, Bernhard, Becker, Kevin W., Dong, Xiaoli, Stairs, Courtney W., Hinrichs, Kai-Uwe, Brown, Matthew W., Roger, Andrew J., Strous, Marc
• Format: Article
• Language: English
• Subjects: 14/28; 14/32; 38/23; 38/91; 631/181/2481; 631/326/171/1878; 692/420/254; 82/58; Animals; Arcobacter - genetics; Arcobacter - physiology; Bacteria; Eukaryota - enzymology; Eukaryota - genetics; Eukaryota - physiology; Genes; Genetic Fitness; Genomes; Harbors; Humanities and Social Sciences; Hydrogen - metabolism; Hydrogenase - genetics; Hydrogenase - metabolism; letter; Microbiological research; multidisciplinary; NADP - metabolism; Nitrous oxide; Phylogenetics; Physiological aspects; Proteins; Proteobacteria; Proteomics; Protista; Science; Symbiosis; Symbiosis - genetics; Transcriptome; Virulence (Microbiology); Virulence - genetics; Virulence Factors - genetics; Virulence Factors - metabolism
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature18297

The cultivation of Lenisia limosa , a newly discovered breviate protist, symbiotically colonized by relatives of the animal-associated bacterium Arcobacter . A 'virulence factor' mediates mutualism This study describes a previously unknown type of mutualistic symbiosis between a newly discovered breviate protist ( Lenisia limosa ) and the animal-associated bacterium Arcobacter spp. Marc Strous and colleagues show that the symbiosis is driven by the transfer of hydrogen and is mutualistic, providing benefits to both partners. The symbiont induces expression of a novel NAD(P)H-accepting hydrogenase, offering a fitness gain to the breviate as the symbiont acts as a hydrogen scavenger. In turn, the breviate induces expression of proteins in the symbiont that seem to be related to classical bacterial virulence factors, acting in this instance to promote the mutualistic relationship. Breviatea form a lineage of free living, unicellular protists, distantly related to animals and fungi 1 , 2 . This lineage emerged almost one billion years ago, when the oceanic oxygen content was low, and extant Breviatea have evolved or retained an anaerobic lifestyle 3 , 4 . Here we report the cultivation of Lenisia limosa , gen. et sp. nov., a newly discovered breviate colonized by relatives of animal-associated Arcobacter . Physiological experiments show that the association of L. limosa with Arcobacter is driven by the transfer of hydrogen and is mutualistic, providing benefits to both partners. With whole-genome sequencing and differential proteomics, we show that an experimentally observed fitness gain of L. limosa could be explained by the activity of a so far unknown type of NAD(P)H-accepting hydrogenase, which is expressed in the presence, but not in the absence, of Arcobacter . Differential proteomics further reveal that the presence of Lenisia stimulates expression of known ‘virulence’ factors by Arcobacter . These proteins typically enable colonization of animal cells during infection 5 , but may in the present case act for mutual benefit. Finally, re-investigation of two currently available transcriptomic data sets of other Breviatea 4 reveals the presence and activity of related hydrogen-consuming Arcobacter , indicating that mutualistic interaction between these two groups of microbes might be pervasive. Our results support the notion that molecular mechanisms involved in virulence can also support mutualism 6 , as shown here for Arcobacter and Breviatea.