Microbial traits and the realized niche in a simple metaorganism

Organisms and their resident microbial communities - the microbiome - form a complex and mostly stable ecosystem. It is known that the specific composition and abundance of certain bacterial species have a major impact on host health and Darwinian fitness, but the processes that lead to these microbial patterns have not yet been identified. We here apply the niche concept and trait-based approaches as a first step in understanding the patterns underlying microbial community assembly and structure in the simple metaorganism Hydra. We find that the carrying capacities in single associations do not reflect microbiota densities as part of the community, indicating a discrepancy between the fundamental and realized niche. Whereas in most cases, the realized niche is smaller than the fundamental one, as predicted by theory, the opposite is observed for Hydra’s two main bacterial colonizers. Both, Curvibacter sp. and Duganella sp. benefit from association with the other members of the microbiome and reach higher fractions as in single colonisations. This cannot be linked to any particular trait that is relevant for interacting with the host or by the utilization of specific nutrients but is most likely determined by metabolic interactions between the individual microbiome members.


43
Microbiomes contribute to ecosystems as key engines that power system-level 44 processes (Falkowski et al., 2008). This also applies to host ecosystems, where they are 45 critical in maintaining host health, survival, and function ( (Kau et

52
The niche concept is one of the core concepts in ecology and has been 53 rediscovered by modern ecology for explaining biodiversity and species coexistence 54 patterns (Pocheville, 2015). The niche-based theory states that an ecological community 55 is made up of a limited number of niches, each occupied by a single species. Hutchinson 56 (Hutchinson, 1957) defined the fundamental niche as the needs of a species for it to 57 maintain a positive population growth rate, disregarding biotic interactions 58 (Hutchinson, 1957;Pearman et al., 2008). The fundamental niche therefore represents 59 an idealized situation exclusive of interspecific interactions. The effect of biological 60 interactions is taken into account in the definition of the realized niche (Hutchinson, 61 1957). This is the portion of the fundamental niche in which a species has a positive 62 population growth rate, despite the constraining effects of biological interactions, such 63 as inter-specific competition (Hutchinson, 1957;Pearman et al., 2008).

64
In the last two decades, the shift from taxonomy to function by using trait-based 65 approaches has provided a detailed understanding of biodiversity-ecosystem 66 functioning (Louca et al., 2018). Recently, this framework is also being used by microbial 67 ecologists to study microbial biogeography (Green et al., 2008), or to unravel microbial 68 biodiversity-ecosystem functioning relationships (Krause et al., 2014). Further, this 69 approach allows studying microbiomes in the light of coexisting traits/ functions rather 70 than of coexisting microbes (Martiny et al., 2015). A recent study successfully used this 71 approach and analysed trait-based patterns to understand the mechanisms of 72 community assembly and succession of the infant gut microbiome (Guittar et al., 2019).

73
Microbial traits cover a range of phenotypic characteristics ranging from simple to 74 complex, for example organic phosphate utilization, bacteriophage host range, cellulose 75 degradation, biofilm formation, nitrogen fixation, methanogenesis, and salinity 76 preference (Martiny et al., 2015). Potential microbial traits can be measured directly by 77 4 laboratory assays (as in this study) or can be indirectly inferred based on genomic 78 information.

79
The aim of this study is to apply the niche concept and trait-based theory to the 80 metaorganism Hydra to gain insight into the mechanisms underlying the microbial 81 community composition. We thus specifically extend the niche-assembly perspective, 82 classically used for assessing species assembly and coexistence in abiotic environments, 83 to a host-associated microbiome, thus a biotic environment.

84
The freshwater polyp and its microbiome have become a valuable model system 85 for metaorganism research as it provides a bridge between the simplicity of synthetic 86 communities and the complex mouse model (Deines and Bosch, 2016

107
Animals used, culture conditions, and generation of germ-free animals 108 Hydra vulgaris (strain AEP) was used in the experiments and cultured according to 109 standard procedures at 18°C in standardized Hydra culture medium (Lenhoff and 110 Brown, 1970). Animals were fed three times a week with 1st instar larvae of Artemia 111 salina. Germ-free polyps were obtained as previously described (Franzenburg et al.,