Parasite Microbiome Project: Systematic Investigation of Microbiome Dynamics within and across Parasite-Host Interactions

Dheilly, Nolwenn M.; Bolnick, Daniel I.; Bordenstein, Seth R.; Brindley, Paul J.; Figuères, Cédric; Holmes, Edward C.; Martínez, Joaquín Martínez; Phillips, Anna J.; Poulin, Robert; Rosario, Karyna

doi:10.1128/msystems.00050-17

Cited by 46 publications

(39 citation statements)

References 22 publications

(22 reference statements)

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“…Although the term "microbiome" is often used in reference to any type of sequencing-based assessment of microbial biodiversity [e.g., the Earth Microbiome Project (Gilbert, Jansson, & Knight, 2014) or the troposphere microbiome (DeLeon-Rodriguez et al, 2013)], the term is most commonly used to define any species found in association with a specific host organism, including known bacterial symbionts [(endo-or ectosymbionts such as Wolbachia or sulphurutilizing bacteria (Ainsworth et al, 2015;Nicks & Rahn-Lee, 2017;Sayavedra et al, 2015;Werren, 1997)] specialized microbial populations that are adapted to life in host-associated habitats such as mucus, gut linings or skin (Glasl, Herndl, & Frade, 2016;Larsen, Bullard, Womble, & Arias, 2015;Schommer & Gallo, 2013;Walke et al, 2017;Walter & Ley, 2011;Weese, 2013), and partially digested gut contents and prey items that can be identified via DNA sequencing (De Barba et al, 2014;Deagle, Kirkwood, & Jarman, 2009;Yu et al, 2012;Zeale, Butlin, Barker, Lees, & Jones, 2011). Common microbiome taxa include both parasitic and commensal species (Dheilly et al, 2017;Nunes-Alves, 2015;Parfrey et al, 2011;Schommer & Gallo, 2013), with host-associated species spanning both prokaryotic and eukaryotic domains of life.…”

Section: Introductionmentioning

confidence: 99%

Nematode‐associated microbial taxa do not correlate with host phylogeny, geographic region or feeding morphology in marine sediment habitats

et al. 2018

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Studies of host-associated microbes are critical for advancing our understanding of ecology and evolution across diverse taxa and ecosystems. Nematode worms are ubiquitous across most habitats on earth, yet little is known about host-associated microbial assemblages within the phylum. Free-living nematodes are globally abundant and diverse in marine sediments, with species exhibiting distinct buccal cavity (mouth) morphologies that are thought to play an important role in feeding ecology and life history strategies. Here, we investigated patterns in marine nematode microbiomes, by characterizing host-associated microbial taxa in 281 worms isolated from a range of habitat types (deep-sea, shallow water, methane seeps, Lophelia coral mounds, kelp holdfasts) across three distinct geographic regions (Arctic, Southern California and Gulf of Mexico). Microbiome profiles were generated from single worms spanning 33 distinct morphological genera, using a two-gene metabarcoding approach to amplify the V4 region of the 16S ribosomal RNA (rRNA) gene targeting bacteria/archaea and the V1-V2 region of the 18S rRNA gene targeting microbial eukaryotes. Contrary to our expectations, nematode microbiome profiles demonstrated no distinct patterns either globally (across depths and ocean basins) or locally (within site); prokaryotic and eukaryotic microbial assemblages did not correlate with nematode feeding morphology, host phylogeny or morphological identity, ocean region or marine habitat type. However, fine-scale analysis of nematode microbiomes revealed a variety of novel ecological interactions, including putative parasites and symbionts, and potential associations with bacterial/archaeal taxa involved in nitrogen and methane cycling. Our results suggest that in marine habitats, free-living nematodes may utilize diverse and generalist foraging strategies that are not correlated with host genotype or feeding morphology. Furthermore, some abiotic factors such as geographic region and habitat type do not appear to play an obvious role in structuring host-microbe associations or feeding preferences.

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Section: Introductionmentioning

confidence: 99%

Nematode‐associated microbial taxa do not correlate with host phylogeny, geographic region or feeding morphology in marine sediment habitats

et al. 2018

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“…The importance of microorganisms as vectors of other microbes or viruses into the holobiome should not be overlooked, given, for example, the role of the protistan root parasite Polymyxa in transmitting a range of pathogenic viruses into crop plants [45]. The pathogenic and functional consequences of hyperparasitic associations have not received much attention (but see, for example, [46]), compounded by the fact that the extent of microbial hyperparasitism is likely underestimated (e.g., [47,48]).…”

Section: Trends In Ecology and Evolutionmentioning

confidence: 99%

The Pathobiome in Animal and Plant Diseases

Bass

Stentiford

Wang

et al. 2019

Trends in Ecology & Evolution

248

189

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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...

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“…The parasitology field is beginning to recognize that parasite-associated microbes, including viruses, can affect parasite fitness and influence the outcome of parasitic infection, and these microbes may be targeted for treatment of parasitic diseases [11][12][13][14][15]. We need to characterize the virome of parasitic organisms to understand the role of parasites in virus evolution and host-microbe interactions, to determine the role of viruses in parasite virulence, and to identify patterns and processes of host-parasite-virus coevolution [14].…”

Section: Introductionmentioning

confidence: 99%

Characterization of viruses in a tapeworm: phylogenetic position, vertical transmission, and transmission to the parasitized host

et al. 2020

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Parasitic flatworms (Neodermata) infect all vertebrates and represent a significant health and economic burden worldwide due to the debilitating diseases they cause. This study sheds light for the first time into the virome of a tapeworm by describing six novel RNA virus candidate species associated with Schistocephalus solidus, including three negative-strand RNA viruses (order Jingchuvirales, Mononegavirales, and Bunyavirales) and three double-stranded RNA viruses. Using in vitro culture of S. solidus, controlled experimental infections and field sampling, we demonstrate that five of these viruses are vertically transmitted, and persist throughout the S. solidus complex life cycle. Moreover, we show that one of the viruses, named Schistocephalus solidus rhabdovirus (SsRV1), is excreted by the parasite and transmitted to parasitized hosts indicating that it may impact S. solidus-host interactions. In addition, SsRV1 has a basal phylogenetic position relative to vertebrate rhabdoviruses suggesting that parasitic flatworms could have contributed to virus emergence. Viruses similar to four of the S. solidus viruses identified here were found in geographically distant S. solidus populations through data mining. Further studies are necessary to determine if flatworm viruses can replicate in parasitized hosts, how they contribute to parasite infection dynamics and if these viruses could be targeted for treatment of parasitic disease.

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Parasite Microbiome Project: Systematic Investigation of Microbiome Dynamics within and across Parasite-Host Interactions

Cited by 46 publications

References 22 publications

Nematode‐associated microbial taxa do not correlate with host phylogeny, geographic region or feeding morphology in marine sediment habitats

Nematode‐associated microbial taxa do not correlate with host phylogeny, geographic region or feeding morphology in marine sediment habitats

The Pathobiome in Animal and Plant Diseases

Characterization of viruses in a tapeworm: phylogenetic position, vertical transmission, and transmission to the parasitized host

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