Large eukaryotes support diverse communities of microbes on their surface—epibiota—that profoundly influence their biology. Alternate factors known to structure complex patterns of microbial diversity—host evolutionary history and ecology, environmental conditions and stochasticity—do not act independently and it is challenging to disentangle their relative effects. Here, we surveyed the epibiota from 38 sympatric seaweed species that span diverse clades and have convergent morphology, which strongly influences seaweed ecology. Host identity explains most of the variation in epibiont communities and deeper host phylogenetic relationships (e.g., genus level) explain a small but significant portion of epibiont community variation. Strikingly, epibiota community composition is significantly influenced by host morphology and epibiota richness increases with morphological complexity of the seaweed host. This effect is robust after controlling for phylogenetic non-independence and is strongest for crustose seaweeds. We experimentally validated the effect of host morphology by quantifying bacterial community assembly on latex sheets cut to resemble three seaweed morphologies. The patterns match those observed in our field survey. Thus, biodiversity increases with habitat complexity in host-associated microbial communities, mirroring patterns observed in animal communities. We suggest that host morphology and structural complexity are underexplored mechanisms structuring microbial communities.

Macroalgae variably promote and deter microbial growth through release of organic carbon and antimicrobial compounds into the water column. Consequently, macroalgae influence the microbial composition of the surrounding water column and biofilms on nearby surfaces. Here, we use manipulative experiments to test the hypotheses that (i) Nereocystis luetkeana and Mastocarpus sp. macroalgae alter the water column microbiota in species-specific manner, that (ii) neighbouring macroalgae alter the bacterial communities on the surface (epibiota) of actively growing Nereocystis luetkeana meristem fragments (NMFs), and that (iii) neighbours alter NMF growth rate. We also assess the impact of laboratory incubation on macroalgal epibiota by comparing each species to wild counterparts. We find strong differences between the Nereocystis and Mastocarpus epibiota that are maintained in the laboratory. Nereocystis and Mastocarpus alter water column bacterial community composition and richness in a species specific manner, but cause only small compositional shifts on NMF surfaces that do not differ by species, and do not change richness. Co-incubation with macroalgae results in significant change in abundance of fivefold more genera in the water column compared to NMF surfaces, although the direction (i.e., enrichment or reduction) of shift is generally consistent between the water and NMF surfaces. Finally, NMFs grew during the experiment, but growth did not depend on the presence or identity of neighbouring macroalgae. Thus, macroalgae exhibit a strong and species-specific influence on the water column microbiota, but a much weaker influence on the epibiota of neighbouring macroalgae. Overall, these results support the idea that macroalgae surfaces are highly selective and demonstrate that modulations of macroalgal microbiota operate within an overarching paradigm of host species specificity.

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Host-associated microbial biofilms can provide protection against pathogen establishment. In many host-microbe symbioses (including, but not limited to: humans, plants, insects, and amphibians), there is a correlation between host-associated microbial diversity and pathogen infection risk. Diversity may prevent infection by pathogens through sampling effects and niche complementarity– but an alternative hypothesis may be that microbial biomass is confounded with diversity, and that host-associated biofilms are deterring pathogen establishment through space pre-emption. In this study, we use the amphibian system as a model for host-microbe-pathogen interactions to ask two questions: (1) is bacterial richness confounded with biofilm thickness or cell density, and (2) to what extent does biofilm thickness, cell density, and bacterial richness each deter the establishment of the amphibian fungal pathogen, Batrachochytrium dendrobatidis (Bd)? To answer these questions, we built a custom biofilm microcosm that mimics the host-environment interface by allowing nutrients to diffuse out of a fine-pore biofilm scaffolding. This created a competitive environment in which bacteria and the fungal pathogen compete for colonization space. We then challenged bacterial biofilms ranging in community richness, biofilm thickness, bacterial cell density, and Bd -inhibitory metabolite production with live Bd zoospores to determine how Bd establishment success on membranes vary. We found that biofilm thickness and Bd -inhibitory isolate richness work in complement to reduce Bd establishment success. This work underscores that physical aspects of biofilm communities can play a large role in pathogen inhibition and in many studies, these traits are not studied. IMPORTANCE Our finding highlights the fact that diversity, as measured through 16S rDNA sequencing, may obscure the true mechanisms behind microbe-mediated pathogen defence, and that physical space occupation by biofilm-forming symbionts may significantly contribute to pathogen protection. These findings have implications across a wide range of host-microbe systems, since 16S rDNA sequencing is a standard tool used across many microbial systems. Further, our results are potentially relevant to many host-pathogen systems, since host-associated bacterial biofilms are ubiquitous.

Host-associated microbes can interact with macro-organisms in a number of ways that affect host health. Few studies of host-associated microbiomes, however, focus on fungi. In addition, it is difficult to discern whether a fungal organism found in or on an ectotherm host is associating with it in a durable, symbiotic interaction versus a transient one, and to what extent the habitat and host share microbes. We seek to identify these host-microbe interactions on an amphibian, the Colorado boreal toad (Anaxyrus boreas boreas). We sequenced the ITS1 region of the fungal community on the skin of wild toads (n = 124) from four sites in the Colorado Rocky Mountains, across its physiologically dynamic developmental life stages. We also sampled the common habitats used by boreal toads: water from their natal wetland and aquatic pond sediment. We then examined diversity patterns within different life stages, between host and habitat, and identified fungal taxa that could be putatively host-associated with toads by using an indicator species analysis on toad versus environmental samples. Host and habitat were strikingly similar, with the exception of toad eggs. Post-hatching toad life stages were distinct in their various fungal diversity measures. We identified eight fungal taxa that were significantly associated with eggs, but no other fungal taxa were associated with other toad life stages compared with their environmental habitat. This suggests that although pre- and post-metamorphic toad life stages differ from each other, the habitat and host fungal communities are so similar that identifying obligate host symbionts is difficult with the techniques used here. This approach does, however, leverage sequence data from host and habitat samples to predict which microbial taxa are host-associated versus transient microbes, thereby condensing a large set of sequence data into a smaller list of potential targets for further consideration.