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

Andrew S Burns,Cody S Clements,Frank J Stewart,Mark E Hay

doi:10.1186/s42523-020-00061-5

Abstract

BackgroundImpacts 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.ResultsIn 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.ConclusionsPrevious 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.

Highlights

Impacts of biotic stressors, such as consumers, on coral microbiomes have gained attention as corals decline worldwide
Analyses of non-rarefied data exhibited similar trends to rarefied data analyses – only differing in that microbiome composition of scars did not significantly differ between outplants hosting 8 mm and 22 mm snails (PERMANOVA, ⍺ = 0.025, p = 0.044) and Random forest analysis indicated that samples from outplants or natural colonies could be predicted with 100% accuracy from bacterial community membership at the exact sequence variant (ESV) level
We found that feeding by the parasitic corallivore C. violacea altered coral microbiomes in ways that may be indicative of dysbiosis

Summary

Introduction

Impacts of biotic stressors, such as consumers, on coral microbiomes have gained attention as corals decline worldwide. 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). Most corallivores are treated as de-facto predators, but corallivory ranges from predators that move among and kill numerous prey to parasites that associate with a single host individual for a long period and seldom kill the host [9] These interactions share conceptual similarities (e.g. consumer-prey interactions [10];), but parasites may cause only modest suppression of host fitness, while mobile predators may kill one or more coral colonies. Sedentary parasites must select prey based on their value as foods, and their suitability as habitats that provide mating sites, refuge from predators, etc. [11]

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