Background: The interplay between hosts and their associated microbiome is now recognized as a fundamental basis of the ecology, evolution, and development of both players. These interdependencies inspired a new view of multicellular organisms as “metaorganisms.” The goal of the Collaborative Research Center “Origin and Function of Metaorganisms” is to understand why and how microbial communities form long-term associations with hosts from diverse taxonomic groups, ranging from sponges to humans in addition to plants. Methods: In order to optimize the choice of analysis procedures, which may differ according to the host organism and question at hand, we systematically compared the two main technical approaches for profiling microbial communities, 16S rRNA gene amplicon and metagenomic shotgun sequencing across our panel of ten host taxa. This includes two commonly used 16S rRNA gene regions and two amplification procedures, thus totaling five different microbial profiles per host sample. Conclusion: While 16S rRNA gene-based analyses are subject to much skepticism, we demonstrate that many aspects of bacterial community characterization are consistent across methods. The resulting insight facilitates the selection of appropriate methods across a wide range of host taxa. Overall, we recommend single- over multi-step amplification procedures, and although exceptions and trade-offs exist, the V3 V4 over the V1 V2 region of the 16S rRNA gene. Finally, by contrasting taxonomic and functional profiles and performing phylogenetic analysis, we provide important and novel insight into broad evolutionary patterns among metaorganisms, whereby the transition of animals from an aquatic to a terrestrial habitat marks a major event in the evolution of host-associated microbial composition.

Animals are usually regarded as independent entities within their respective environments. However, within an organism, eukaryotes and prokaryotes interact dynamically to form the so-called metaorganism or holobiont, where each partner fulfils its versatile and crucial role. This review focuses on the interplay between microorganisms and multicellular eukaryotes in the context of host physiology, in particular aging and mucus-associated crosstalk. In addition to the interactions between bacteria and the host, we highlight the importance of viruses and nonmodel organisms. Moreover, we discuss current culturing and computational methodologies that allow a deeper understanding of underlying mechanisms controlling the physiology of metaorganisms.

Significance: A central goal in invasion genomics is to identify and determine the mechanisms that underlie the successful colonization, establishment, and subsequent range expansion of invasive populations of nonindigenous species. Using a whole-genome approach, we evaluate the importance of genetic diversity for the successful establishment of nonindigenous species. Our study shows that genetic diversity per se is not the major factor driving invasions, since we observed all possible scenarios with invasive populations showing reduced, similar but also increased, genetic diversity relative to the native population. Using coalescent methods, we reconstruct the demographic history of the invasion and infer the source population of each invasion event, which shows that propagule pressure and multiple introductions play an important role in determining invasion success.

The ctenophore Mnemiopsis leidyi is characterized by high growth rates and a large reproductive capacity. However, reproductive dynamics are not yet well understood. Here, we present laboratory data on food-dependent egg production in M. leidyi and egg hatching time and success. Further, we report on the reproduction of laboratory-reared and field-caught animals during starvation. Our results show that the half-saturation zooplankton prey concentration for egg production is reached at food levels of 12–23 µgC L⁻¹, which is below the average summer food concentration encountered in invaded areas of northern Europe. Furthermore, starved animals continue to produce eggs for up to 12 days after cessation of feeding with high overall hatching success of 65–90%. These life history traits allow M. leidyi to thrive and reproduce in environments with varying food conditions and give it a competitive advantage under unfavourable conditions. This may explain why recurrent population blooms are observed and sustained in localized areas in invaded northern Europe, where water exchange is limited and zooplankton food resources are quickly depleted by M. leidyi. We suggest that these reproductive life history traits are key to its invasion success.

The recent invasion of the comb jelly Mnemiopsis leidyi into northern European waters is of major public and scientific concern. One of the key features making M. leidyi a successful invader is its high fecundity combined with fast growth rates. However, little is known about physiological limitations to its reproduction and consequent possible abiotic restrictions to its dispersal. To evaluate the invasion potential of M. leidyi into the brackish Baltic Sea we studied in situ egg production rates in different regions and at different salinities in the laboratory, representing the salinity gradient of the Baltic Sea. During October 2009 M. leidyi actively reproduced over large areas of the Baltic Sea. Egg production rates scaled with animal size but decreased significantly with decreasing salinity, both in the field (7–29) and in laboratory experiments (6–33). Temperature and zooplankton, i.e. food abundance, could not explain the observed differences. Reproduction rates at conditions representing the Kattegat, south western and central Baltic Sea, respectively, were 2.8 fold higher at the highest salinities (33 and 25) than at intermediate salinities (10 and 15) and 21 times higher compared from intermediate to the lowest salinity tested (6). Higher salinity areas such as the Kattegat, and to a lower extent the south western Baltic, seem to act as source regions for the M. leidyi population in the central Baltic Sea where a self-sustaining population, due to the low salinity, cannot be maintained.