Pathogen resistance may be the principal evolutionary advantage provided by the microbiome

McLaren, Michael R.; Callahan, Benjamin J.

doi:10.1098/rstb.2019.0592

Cited by 87 publications

(55 citation statements)

References 84 publications

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“…Pathogen resistance is a noted advantage provided by GM [60], which is also expected to provide protection against NEC. Using Pearson's correlation analysis, we found the shifted abundance of Cl.…”

Section: Discussionmentioning

confidence: 99%

Donor-dependent Fecal Microbiota Transplantation Efficacy Against Necrotizing Enterocolitis in Preterm Pigs

Hui¹,

Vestergaard²,

Deng³

et al. 2020

Preprint

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BackgroundFecal microbiota transplantation (FMT) has shown high cure rates against recurrent Clostridioides difficile infection regardless of donor microbiota characteristics, whereas the clinical response of FMT in inflammatory bowel disease appears to be donor-dependent. We recently showed that FMT from healthy suckling piglet donors to newborn preterm piglets decreased the risk of necrotizing enterocolitis (NEC), a serious gastrointestinal disease of preterm infants, but could not replicate this finding in a follow-up study using phenotypically similar donors. This gave us the opportunity to directly investigate the microbiota dynamics of clinically efficient FMT. In this experiment, preterm piglets (n=38) were randomly allocated to receive control saline or FMT from inferior (FMT1) or superior donors (FMT2) by rectal administration. All animals were fed infant formula for four days to induce NEC-like lesions before necropsy and gut pathological evaluation. Donor and recipient colonic microbiotas were analyzed by 16S rRNA gene amplicon sequencing and shotgun metagenomics.ResultsAlthough the two donor microbiotas closely resembled one another, only FMT2 recipients had improved body growth and lower intestinal permeability relative to control, and were protected against NEC. Both FMT groups had shifted colon microbiota composition relative to CON, with increased lactobacilli relative abundance, but FMT2 recipients had a higher lactobacilli abundance relative to FMT1. Limosilactobacillus reuteri and Lactobacillus crispatus strains of FMT recipients showed high phylogenetic similarity with their respective donors, indicating successful engraftment. Further, NEC severity was positively associated with Clostridoides difficile, Clostridium perfringens and Enterococcus faecium abundance, while Lmb. reuteri and Lb. crispatus negatively correlated with diarrhea severity. Genome-resolved analysis indicated a higher gut replication rate of lactobacilli in FMT2 recipients, and identified specific glycosaminoglycan-degrading Bacteroides in the superior donor.ConclusionsFMT efficacy against NEC is donor-dependent, and introduced lactobacilli manifest strain-level differences with respect to colonizing recipients. Using shotgun metagenomics, we traced the engrafted strains back from donors and identified donor-specific microbes of potential importance. This may accelerate our understanding of optimal donor selection for clinical FMT.

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Section: Discussionmentioning

confidence: 99%

Donor-dependent Fecal Microbiota Transplantation Efficacy Against Necrotizing Enterocolitis in Preterm Pigs

Hui¹,

Vestergaard²,

Deng³

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…Marine organisms have evolved complex structural, behavioral, and chemical mechanisms to regulate the presence, abundance, and activity of their microbial associates. Hosts can limit colonization by transient opportunistic microbes that would use space and resources without providing any benefits, and some hosts can even block pathogens entirely [ 17 – 19 ]. Host-specific and obligate microbial associates, often called the “core microbiome” of a host population or species, are generally assumed to play more important functional roles than opportunistic and transient taxa [ 20 ].…”

Section: Mainmentioning

confidence: 99%

Natural experiments and long-term monitoring are critical to understand and predict marine host–microbe ecology and evolution

et al. 2021

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Marine multicellular organisms host a diverse collection of bacteria, archaea, microbial eukaryotes, and viruses that form their microbiome. Such host-associated microbes can significantly influence the host’s physiological capacities; however, the identity and functional role(s) of key members of the microbiome (“core microbiome”) in most marine hosts coexisting in natural settings remain obscure. Also unclear is how dynamic interactions between hosts and the immense standing pool of microbial genetic variation will affect marine ecosystems’ capacity to adjust to environmental changes. Here, we argue that significantly advancing our understanding of how host-associated microbes shape marine hosts’ plastic and adaptive responses to environmental change requires (i) recognizing that individual host–microbe systems do not exist in an ecological or evolutionary vacuum and (ii) expanding the field toward long-term, multidisciplinary research on entire communities of hosts and microbes. Natural experiments, such as time-calibrated geological events associated with well-characterized environmental gradients, provide unique ecological and evolutionary contexts to address this challenge. We focus here particularly on mutualistic interactions between hosts and microbes, but note that many of the same lessons and approaches would apply to other types of interactions.

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“…Commensal microbes that have evolved within the host could contribute to the overall pathogen resistance of the host through competition with pathogens for resources and via direct inhibition. According to some authors, this cooperative immunity, which facilitates the adaptive evolution of non-pathogen-related host traits, is the principal evolutionary advantage provided by the microbiome to their host (McLaren and Callahan, 2020).…”

Section: Evolution and Adaptationmentioning

confidence: 99%

Corals and Sponges Under the Light of the Holobiont Concept: How Microbiomes Underpin Our Understanding of Marine Ecosystems

et al. 2021

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In the past 20 years, a new concept has slowly emerged and expanded to various domains of marine biology research: the holobiont. A holobiont describes the consortium formed by a eukaryotic host and its associated microorganisms including bacteria, archaea, protists, microalgae, fungi, and viruses. From coral reefs to the deep-sea, symbiotic relationships and host–microbiome interactions are omnipresent and central to the health of marine ecosystems. Studying marine organisms under the light of the holobiont is a new paradigm that impacts many aspects of marine sciences. This approach is an innovative way of understanding the complex functioning of marine organisms, their evolution, their ecological roles within their ecosystems, and their adaptation to face environmental changes. This review offers a broad insight into key concepts of holobiont studies and into the current knowledge of marine model holobionts. Firstly, the history of the holobiont concept and the expansion of its use from evolutionary sciences to other fields of marine biology will be discussed. Then, the ecology and physiology of marine holobionts will be investigated through the examples of corals and sponges. We will discuss the impacts of environmental change on organisms at the holobiont level and how microbiomes contribute to the resilience and/or vulnerability of their host in the face of environmental stressors. Finally, we will conclude with the development of new technologies, holistic approaches, and future prospects for conservation biology surrounding marine holobionts.

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Pathogen resistance may be the principal evolutionary advantage provided by the microbiome

Cited by 87 publications

References 84 publications

Donor-dependent Fecal Microbiota Transplantation Efficacy Against Necrotizing Enterocolitis in Preterm Pigs

Donor-dependent Fecal Microbiota Transplantation Efficacy Against Necrotizing Enterocolitis in Preterm Pigs

Natural experiments and long-term monitoring are critical to understand and predict marine host–microbe ecology and evolution

Corals and Sponges Under the Light of the Holobiont Concept: How Microbiomes Underpin Our Understanding of Marine Ecosystems

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