Search

Animal development has traditionally been viewed as an autonomous process directed by the host genome. But in many animals biotic and abiotic cues, like temperature and bacterial colonizers, provide signals for multiple developmental steps. Hydra offers unique features to encode these complex interactions of developmental processes with biotic and abiotic factors. Here, we used the model animal Hydra to investigate the impact of bacterial colonizers and temperature on the pattern formation process. In Hydra, formation of the head organizer involves the canonical Wnt pathway. Treatment with alsterpaullone (ALP) results in acquiring characteristics of the head organizer in the body column. Intriguingly, germ-free Hydra polyps are significantly more sensitive to ALP compared to control polyps. In addition to microbes, β-catenin dependent pattern formation is also affected by temperature. Gene expression analyses led to the identification of two small secreted peptides, named Eco1 and Eco2, being upregulated in the response to both, Curvibacter sp, the main bacterial colonizer of Hydra, and low temperatures. Loss-of function experiments revealed that Eco peptides are involved in the regulation of pattern formation and have an antagonistic function to Wnt signaling in Hydra.

Current research highlights the importance of associated microbes in contributing to the functioning, health, and even adaptation of their animal, plant, and fungal hosts. As such, we are witnessing a shift in research that moves away from focusing on the eukaryotic host sensu stricto to research into the complex conglomerate of the host and its associated microorganisms (i.e., microbial eukaryotes, archaea, bacteria, and viruses), the so-called metaorganism, as the biological entity. While recent research supports and encourages the adoption of such an integrative view, it must be understood that microorganisms are not involved in all host processes and not all associated microorganisms are functionally important. As such, our intention here is to provide a critical review and evaluation of perspectives and limitations relevant to studying organisms in a metaorganism framework and the functional toolbox available to do so. We note that marker gene-guided approaches that primarily characterize microbial diversity are a first step in delineating associated microbes but are not sufficient to establish proof of their functional relevance. More sophisticated tools and experiments are necessary to reveal the specific functions of associated microbes. This can be accomplished through the study of metaorganisms in less complex environments, the targeted manipulation of microbial associates, or work at the mechanistic level with the toolbox available in model systems. We conclude that the metaorganism framework is a powerful new concept to help provide answers to longstanding biological questions such as the evolution and ecology of organismal complexity and the importance of organismal symbioses to ecosystem functioning. The intricacy of the metaorganism requires a holistic framework combining reductionist and integrative approaches to resolve metaorganism identities and to disclose the various roles that microorganisms play in the biology of their hosts.

It is now recognised that the biology of almost any organism cannot be fully understood without recognising the existence and potential functional importance of associated microbes. Arguably, the emergence of this holistic viewpoint may never have occurred without the development of a crucial molecular technique, 16S rDNA gene amplicon sequencing, which allowed microbial communities to be easily profiled across a broad range of contexts. A diverse array of molecular techniques are now used to profile microbial communities, infer their evolutionary histories, visualise them in host tissues, and measure their molecular activity. In this review, we examine each of these categories of measurement and inference with a focus on the questions they make tractable, and the degree to which their capabilities and limitations shape our view of the holobiont. published

Supplementary Materials. (PDF 6900 kb)

Microbial communities are accompanied by a diverse array of viruses. Through infections of abundant microbes, these viruses have the potential to mediate competition within the community, effectively weakening competitive interactions and promoting coexistence. This is of particular relevance for host-associated microbial communities, because the diversity of the microbiota has been linked to host health and functioning. Here, we study the interaction between two key members of the microbiota of the freshwater metazoan Hydra vulgaris. The two commensal bacteria Curvibacter sp. and Duganella sp. protect their host from fungal infections, but only if both of them are present. Coexistence of the two bacteria is thus beneficial for Hydra. Intriguingly, Duganella sp. appears to be the superior competitor in vitro due to its higher growth rate when both bacteria are grown separately, but in co-culture the outcome of competition depends on the relative initial abundances of the two species. The presence of an inducible prophage in the Curvibacter sp. genome, which is able to lytically infect Duganella sp., led us to hypothesize that the phage modulates the interaction between these two key members of the Hydra microbiota. Using a mathematical model, we show that the interplay of the lysogenic life cycle of the Curvibacter phage and the lytic life cycle on Duganella sp. can explain the observed complex competitive interaction between the two bacteria. Our results highlight the importance of taking lysogeny into account for understanding microbe–virus interactions and show the complex role phages can play in promoting coexistence of their bacterial hosts.