Arthropod–bacteria interactions influence assembly of aquatic host microbiome and pathogen defense

Abstract

The host-associated microbiome is vital to host immunity and pathogen defense. In aquatic ecosystems, organisms may interact with environmental bacteria to influence the pool of potential symbionts, but the effects of these interactions on host microbiome assembly and pathogen resistance are unresolved. We used replicated bromeliad microecosystems to test for indirect effects of arthropod–bacteria interactions on host microbiome assembly and pathogen burden, using tadpoles and the fungal amphibian pathogen Batrachochytrium dendrobatidis as a model host–pathogen system. Arthropods influenced host microbiome assembly by altering the pool of environmental bacteria, with arthropod–bacteria interactions specifically reducing host colonization by transient bacteria and promoting antimicrobial components of aquatic bacterial communities. Arthropods also reduced fungal zoospores in the environment, but fungal infection burdens in tadpoles corresponded most closely with arthropod-mediated patterns in microbiome assembly. This result indicates that the cascading effects of arthropods on the maintenance of a protective host microbiome may be more strongly linked to host health than negative effects of arthropods on pools of pathogenic zoospores. Our work reveals tight links between healthy ecosystem dynamics and the functioning of host microbiomes, suggesting that ecosystem disturbances such as loss of arthropods may have downstream effects on host-associated microbial pathogen defenses and host fitness.

Microbiome Shifts Associated With the Introduction of Wild Atlantic Horseshoe Crabs (Limulus polyphemus) Into a Touch-Tank Exhibit

“…An ever-increasing body of literature has demonstrated the importance of diverse microorganisms in ecology, such as biogeochemical cycling ( Rousk and Bengtson, 2014 ), ecosystem health ( Hooper et al, 2005 ), and disease prevention in hosts ( Hamdi et al, 2011 ; Greenspan et al, 2019 ). In our study, we documented a drastic decrease in the diversity of the wild-caught horseshoe crabs microbiome and significant shifts in microbial community structure shortly after entering captivity.…”

Diversity-Stability Dynamics of the Amphibian Skin Microbiome and Susceptibility to a Lethal Viral Pathogen

“…their skin microbiomes provide a model for understanding the processes shaping the forces of colonization, competition and coexistence of microbial species on a vertebrate host, and quantifying the emergent functional properties of these microbial communities and their consequences for the host. The properties of this system make it well suited to testing the applicability of established ecological theory derived from eukaryotic communities to prokaryotic assemblages associated with animals, plants and soils, including the relationship between biodiversity and ecosystem function (e.g., see Koskella et al, 2017;Greenspan et al, 2019).…”

“…Anti-fungal metabolite production by bacteria increases dramatically when the bacteria are co-cultured (Loudon et al, 2014a), suggesting that microbiome-mediated host protection is likely a function of synergistic interactions among community members. Greater microbiome diversity may therefore offer increased protection from pathogens (e.g., Piovia-Scott et al, 2017;Antwis and Harrison, 2018;Greenspan et al, 2019; but see Becker et al, 2019), but the ecological processes structuring and maintaining microbial diversity on amphibian skin remain relatively understudied, especially at the level of the individual (Loudon et al, 2014b(Loudon et al, , 2016Longo and Zamudio, 2017;Hughey et al, 2019). For example, the diversitystability hypothesis predicts that more diverse communities should be more resistant to disturbance, and several empirical studies support this hypothesis in plant community assemblages (McCann, 2000;Costello et al, 2012), but it is unclear whether this theory is also relevant at the scale of host-associated microbial communities (Costello et al, 2012, but see Koskella et al, 2017).…”

Skin microbiome correlates with bioclimate and Batrachochytrium dendrobatidis infection intensity in Brazil’s Atlantic Forest treefrogs

“…Both environmental and host-specific factors are predictors of amphibian skin microbiome structure 18 , 19 . Among the environmental factors influencing the cutaneous bacterial communities of amphibians, life stage transitions 18 , 20 , 21 , diet composition 22 , disease 23 , elevation 24 , microbial interactions 25 , 26 , season 17 , 27 , temperature 14 , water pH 28 , contaminants 28 , captivity 29 , 30 , habitat fragmentation 31 , 32 , trophic network interactions 33 , host assemblages 34 , and precipitation have been identified 35 . Host associated factors are less studied but clearly also play a role because multiple studies have demonstrated that the skin microbiomes of co-occurring species are significantly different 18 , 29 , 36 , 37 .…”