Parasite-host ecology: the limited impacts of an intimate enemy on host microbiomes

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Clements et al. Animal Microbiome (2020) 2:42 https://doi.org/10.1186/s42523-020-00061-5

RESEARCH ARTICLE

Open Access

Parasite-host ecology: the limited impacts of an intimate enemy on host microbiomes Cody S. Clements1* , Andrew S. Burns1,2, Frank J. Stewart1,3 and Mark E. Hay1

Abstract Background: Impacts of biotic stressors, such as consumers, on coral microbiomes have gained attention as corals decline worldwide. Corallivore feeding can alter coral microbiomes in ways that contribute to dysbiosis, but feeding strategies are diverse – complicating generalizations about the nature of consumer impacts on coral microbiomes. Results: In field experiments, feeding by Coralliophila violacea, a parasitic snail that suppresses coral growth, altered the microbiome of its host, Porites cylindrica, but these impacts were spatially constrained. Alterations in microbial community composition and variability were largely restricted to snail feeding scars; basal or distal areas ~ 1.5 cm or 6–8 cm away, respectively, were largely unaltered. Feeding scars were enriched in taxa common to stressed corals (e.g. Flavobacteriaceae, Rhodobacteraceae) and depauperate in putative beneficial symbionts (e.g. Endozoicomonadaceae) compared to locations that lacked feeding. Conclusions: Previous studies that assessed consumer impacts on coral microbiomes suggested that feeding disrupts microbial communities, potentially leading to dysbiosis, but those studies involved mobile corallivores that move across and among numerous individual hosts. Sedentary parasites like C. violacea that spend long intervals with individual hosts and are dependent on hosts for food and shelter may minimize damage to host microbiomes to assure continued host health and thus exploitation. More mobile consumers that forage across numerous hosts should not experience these constraints. Thus, stability or disruption of microbiomes on attacked corals may vary based on the foraging strategy of coral consumers. Keywords: Coral reefs, Coralliophila, Corallivore, Gastropod, Microbial interactions, Parasite-host interactions, Parasitism

Background Tropical coral reefs are among Earth’s most biodiverse and productive ecosystems, but corals are in precipitous global decline due to a variety of physical and biotic stressors [1, 2]. The magnitude and spatial scale of these stressors are diverse – ranging from ocean-scale impacts of global change to interactions between individual corals and their associated microbes [3]. The latter have gained considerable interest, because microbial associates play both positive (e.g. nutrient uptake, pathogen resistance) * Correspondence: [email protected] 1 Aquatic Chemical Ecology Center, and Center for Microbial Dynamics and Infection, School of Biological Sciences, Georgia Institute of Technology, 950 Atlantic Drive, Atlanta, GA 30332-0230, USA Full list of author information is available at the end of the article

and negative (e.g. disease) roles in coral health [4, 5]. Additionally, stressor-induced changes to microbiomes have