The Pathobiome in Animal and Plant Diseases

Abstract

A growing awareness of the diversity and ubiquity of microbes (eukaryotes, prokaryotes, and viruses) associated with larger 'host' organisms has led to the realisation that many diseases thought to be caused by one primary agent are the result of interactions between multiple taxa and the host. Even where a primary agent can be identified, its effect is often moderated by other symbionts. Therefore, the one pathogen-one disease paradigm is shifting towards the pathobiome concept, integrating the interaction of multiple symbionts, host, and environment in a new understanding of disease aetiology. Taxonomically, pathobiomes are variable across host species, ecology, tissue type, and time. Therefore, a more functionally driven understanding of pathobiotic systems is necessary, based on gene expression, metabolic interactions, and ecological processes. Disease in a Microbe-Dominated World The pathobiome (see Glossary) concept arose from human studies in which disruption of a healthpromoting and ecologically stable gut microbiome resulted in dysbiosis: a microbiome community of low-diversity and modified metabolic state, exposing the gut to invasion by, and proliferation of, pathogenic agents [1,2]. Dysbiotic communities can subvert the immune system and lead to further deleterious effects [3]. This concept is being adopted for research into the pathology of other animals and plants because attempts to explain syndromic conditions by identifying a single pathogenic agent are often incomplete (i.e., the one pathogen-one disease paradigm is often insufficient to explain many diseases [4-6]). Pathobiomes differ from those assemblages representing healthy or 'normal' states. What is 'normal' likely encompasses a range of assemblages that need to be understood before a pathobiome can be reliably distinguished from them. There is a lack of consistency in defining 'pathobiome' in the literature, ranging from a single pathogenic agent interacting with its biotic and abiotic environments (e.g., [5]) to the effects of interacting communities of microbes on host health [7]. Our synthesis (Box 1) is based on the effects of multiple symbionts, across all domains of life, on host health. The term 'microbiome' generally excludes eukaryotes; therefore, in this review, we use the term 'symbiome' to describe the whole assemblage of associated organisms excluding the host, and 'symbiont' for individual taxa within that assemblage. This definition is concordant with an inclusive scheme of symbiosis acknowledged in [9], which ranges from neutralism (neutral effect on both partners) to mutual beneficial effects and mutual antagonistic effects, and all other possible combinations of neutral, beneficial, and antagonistic effects. The duration of the association need not necessarily be long-term, as interactions can be effective on even short timescales; great variability in duration of association is both possible and likely. This inclusive definition is not inconsistent with some previous usages of the term, and is required by the large div...

Rhizosphere protists are key determinants of plant health

“…2d). This suggests that a pathobiome forms in diseased plants [34,35], here consisting of a simultaneous infection with different pathogens. While, a dominance of predator-prey interactions might mitigate negative pathogen effects and thereby stimulating plant health.…”

Microbial association networks give relevant insights into plant pathobiomes

“…A paradigm shift occurred in 2014 with the integration of the microbiota into this framework (Vayssier-Taussat et al 2014;Kemen et al 2015;Vandenkoornhuyse et al 2015). The new paradigm led to the concept of the pathobiome, which corresponds to all the microorganisms associated with a host that regulate disease (Vayssier-Taussat et al 2014;Brader et al 2017;Bass et al 2019). Contemporaneous meta-barcoding and meta-genomic approaches revealed the huge microbial diversity associated with soil and plants, including grapevine (Zarraonaindia et al 2015).…”

“…Plant growth and health depend on their associations with a large number of microorganisms that interact with each other (Vandenkoornhuyse et al 2015;Hassani et al 2018). Among all these microorganisms, those that interact with pathogens and regulate diseases are particularly important and were recently termed the plant's pathobiome (Vayssier-Taussat et al 2014;Brader et al 2017;Bass et al 2019). Some pathobiome members form a barrier that limits pathogen development through direct antagonistic interactions (Arnold et al 2003;Kemen 2014;Durán et al 2018;Li et al 2019), while others can prime the plant immune system (Vogel et al 2016;Lee et al 2017;Hacquard et al 2017).…”

Phyllosphere Microbiome in Response to Citrus Melanose

“…Cyphellophora and Colletotrichum) (Additional le 2: Table S5) [13,33]. Recent studies found that attempts to explain the occurrence of diseases by identifying single pathogens often represented incomplete understanding of the true causes [34]. Instead, synergistic interactions among multiple microbial pathogens may represent the prevalent pattern in nature [35].…”