Abstract
Our understanding of diseases has been transformed by the realisation that people are holobionts, comprised of a host and its associated microbiome(s). Disease can also have devastating effects on populations of marine organisms, including dominant habitat formers such as seaweed holobionts. However, we know very little about how interactions between microorganisms within microbiomes - of humans or marine organisms – affect host health and there is no underpinning theoretical framework for exploring this. We applied ecological models of succession to bacterial communities to understand how interactions within a seaweed microbiome affect the host. We observed succession of surface microbiomes on the red seaweed Delisea pulchra in situ, following a disturbance, with communities ‘recovering’ to resemble undisturbed states after only 12 days. Further, if this recovery was perturbed, a bleaching disease previously described for this seaweed developed. Early successional strains of bacteria protected the host from colonisation by a pathogenic, later successional strain. Host chemical defences also prevented disease, such that within-microbiome interactions were most important when the host’s chemical defences were inhibited. This is the first experimental evidence that interactions within microbiomes have important implications for host health and disease in a dominant marine habitat-forming organism.
Highlights
Disease is emerging as a fundamentally important factor affecting the ecology and evolution of higher organisms by exerting profound effects on host performance, fitness and/or survival[1,2,3]
Data from experiment 1 were used to create a cyclic model of community shifts and microbial community changes in the disturbed D. pulchra treatments in subsequent experiments were tested against this model
Despite the poor fit in this instance, the cyclic shift is clearly evident in the nMDS plot from this experiment and overall, cyclic change in microbial communities was consistently observed among the disturbed D. pulchra treatments in all experiments
Summary
Disease is emerging as a fundamentally important factor affecting the ecology and evolution of higher organisms by exerting profound effects on host performance, fitness and/or survival[1,2,3]. The holobiont approach involves assessing the health of a host organism in the context of its associated microbiome(s)[10,11] and studies supporting the interdependence of macro- and microbiota within holobionts have recently emerged for diverse organisms including humans[11] and demonstrate a clear association between shifts in the composition of microbiomes and disease in the host[12,13,14,15]. These observations imply that interactions within microbiomes are important for their hosts. We apply succession theory to understand how microbiomes associated with naturally occurring macroalgae change following an experimental disturbance in situ and whether interactions between microorganisms within microbiomes can affect disease incidence or severity in the host
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