Host derived mechanisms controlling bacterial colonization at the epithelial interface in the basal metazoan Hydra
Final Report Abstract
Part I -AMPs represent an important regulatory mechanism to shape the composition of commensal bacteria. The innate immune system as the host’s first line of contact with the microbiota is expected to play a crucial role in the selection of the microbiota. AMPs are important effectors of innate immunity throughout the animal kingdom. However, more and more hints have been accumulated that AMPs are not only killers but are a selecting force and maintenance factor for stable microbial communities. Therefore, I proposed that the secretion of specific AMPs reflects a habitat-specific adaptation to control habitat-specific bacterial colonizers. As a case study, we investigated the role of the arminin gene family, a potent antimicrobial peptide family in Hydra in shaping the species-specific bacterial colonization. We were able to detect by large transcriptome sequencing arminin genes in four Hydra species, with each species possessing a unique composition and expression profile of certain arminin family members. For functional analysis, we established arminin-deficient polyps and in contrast to control polyps, these polyps displayed a decreased potential to select for bacterial communities resembling their native microbiota. This indicates that species-specific antimicrobial peptides shape species-specific bacterial associations and present host-derived regulators of microbial diversity rather than unselective bacteriocides. Part II – Hydra modifies bacterial quorum sensing and thereby control symbiotic functions of its colonizers. Every metaorganism consisting of the host and its associated microbes needs to maintain its homeostasis. Bacteria itself are able to control community wide behavior by quorum sensing (QS), a bacterial communication mechanisms regulating among others biofilm formation, virulence and motility. Here we show that Hydra polyps regulate the behavior of its bacterial colonizers by interfering with their QS system. We could prove that six commensal bacteria of Hydra vulgaris (AEP), representing 90% of the bacterial community, are producing N-acyl-homoserine-lactones (AHLs), a class of bacterial signaling molecules involved in QS of gram-negative bacteria. In contrast, we could identify a new host mechanism, which enables Hydra to modify specifically long-chain 3-oxo-HSLs via an oxidoreductase activity to the 3-hydroxy-HSL counterpart. Interestingly, investigating the impact of AHL-modification on metaorganism assembly in vivo revealed, that the host-modified 3-hydroxy-HSL promotes, while the non-modified 3-oxo-HSL represses symbiont colonization of the host. Furthermore, transcriptional expression data revealed that the main bacterial colonizer Curvibacter sp. possess a differential response to the host-modified 3-hydroxy-HSL compared to the non-modified 3- oxo-HSL. Genes involved in flagella biosynthesis were significantly induced by the non-modified 3- oxo-HSL, leading to swarming behavior of Curvibacter in vivo. These insights show for the first time, that a host organism is modifying bacterial QS signals in vivo and thereby contribute to the homeostasis of the metaorganism.
Publications
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(2013) Distinct antimicrobial peptide expression determines host species-specific bacterial associations. Proc Natl Acad Sci USA, 110(39):E3730-8
Franzenburg S, Walter J, Künzel S, Wang J, Baines JF, Bosch TCG, Fraune S
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(2015) Bacteria-bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance. ISME J. 9:1543-56
Fraune S, Anton-Erxleben F, Augustin R, Franzenburg S, Knop M, Schröder K, Willoweit-Ohl D, and Bosch TCG
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(2015) Which games are growing bacterial populations playing? J. Royal Society Interface
Li XY, Pietschke C, Fraune S, Altrock PM, Bosch TCG, Traulsen A
