Microbiome interactions shape host fitness

Gould, Alison L.; Zhang, Vivian; Lamberti, Lisa; Jones, Eric; Obadia, Benjamin; Korasidis, Nikolaos; Gavryushkin, Alex; Carlson, Jean M.; Beerenwinkel, Niko; Ludington, William B.

doi:10.1073/pnas.1809349115

Cited by 461 publications

(531 citation statements)

References 40 publications

(60 reference statements)

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“…The environmental characters responsible for the variation could include temperature or diet (Chandler et al, 2011;Moghadam et al, 2018;Staubach et al, 2013), and at least some genetic factors that shape the microbiota composition of D. melanogaster have been described (Broderick, Buchon, & Lemaitre, 2014;Dobson et al, 2015). An additional or alternative explanation is that the characteristics described for laboratory flies may not reflect the biology of wild flies, since the interactions of Drosophila and their microbiota can vary depending if the partners are from the wild or the laboratory (Blum, Fischer, Miles, & Handelsman, 2013;Gould et al, 2018;Inamine et al, 2018;Obadia et al, 2017;Pais, Valente, Sporniak, & Teixeira, 2018;Winans et al, 2017). Therefore, we cannot rule out that characteristics defining interactions between laboratory Drosophila and their microbiota, such as inconstancy, are different for laboratory and wild flies.…”

Section: Discussionmentioning

confidence: 99%

The microbiota influences the Drosophila melanogaster life history strategy

et al. 2020

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Organisms are locally adapted when members of a population have a fitness advantage in one location relative to conspecifics in other geographies. For example, across latitudinal gradients, some organisms may trade off between traits that maximize fitness components in one, but not both, of somatic maintenance or reproductive output. Latitudinal gradients in life history strategies are traditionally attributed to environmental selection on an animal's genotype, without any consideration of the possible impact of associated microorganisms (“microbiota”) on life history traits. Here, we show in Drosophila melanogaster, a key model for studying local adaptation and life history strategy, that excluding the microbiota from definitions of local adaptation is a major shortfall. First, we reveal that an isogenic fly line reared with different bacteria varies the investment in early reproduction versus somatic maintenance. Next, we show that in wild fruit flies, the abundance of these same bacteria was correlated with the latitude and life history strategy of the flies, suggesting geographic specificity of the microbiota composition. Variation in microbiota composition of locally adapted D. melanogaster could be attributed to both the wild environment and host genetic selection. Finally, by eliminating or manipulating the microbiota of fly lines collected across a latitudinal gradient, we reveal that host genotype contributes to latitude‐specific life history traits independent of the microbiota and that variation in the microbiota can suppress or reverse the differences between locally adapted fly lines. Together, these findings establish the microbiota composition of a model animal as an essential consideration in local adaptation.

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Section: Discussionmentioning

confidence: 99%

The microbiota influences the Drosophila melanogaster life history strategy

et al. 2020

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“…Therefore, a suitable research strategy and model for studying the interaction of intestinal flora is required to facilitate a clarification of the characteristics of the intestinal flora ecology . A study of Drosophila melanogaster shows that interactions between bacterial species can affect host life and microbial abundance . It is possible that multi‐omic microbiome interactions may underlie UC disease activity.…”

Section: Ecological Imbalance Of Intestinal Flora In Ucmentioning

confidence: 99%

Gut microbiota in ulcerative colitis: insights on pathogenesis and treatment

Guo

Liu

Hao

2020

J of Digest Diseases

174

110

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Gut microbiota constitute the largest reservoir of the human microbiome and are an abundant and stable ecosystem—based on its diversity, complexity, redundancy, and host interactions This ecosystem is indispensable for human development and health. The integrity of the intestinal mucosal barrier depends on its interactions with gut microbiota. The commensal bacterial community is implicated in the pathogenesis of inflammatory bowel disease (IBD), including ulcerative colitis (UC). The dysbiosis of microbes is characterized by reduced biodiversity, abnormal composition of gut microbiota, altered spatial distribution, as well as interactions among microbiota, between different strains of microbiota, and with the host. The defects in microecology, with the related metabolic pathways and molecular mechanisms, play a critical role in the innate immunity of the intestinal mucosa in UC. Fecal microbiota transplantation (FMT) has been used to treat many diseases related to gut microbiota, with the most promising outcome reported in antibiotic‐associated diarrhea, followed by IBD. This review evaluated the results of various reports of FMT in UC. The efficacy of FMT remains highly controversial, and needs to be regularized by integrated management, standardization of procedures, and individualization of treatment.

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“…Macro‐organisms harbour complex microbial communities living inside and on their body (Margulis, ; Theis et al, ). These microbial communities, known as the microbiomes, can determine pivotal phenotypic traits of their hosts, driving a variety of ecological and evolutionary processes including major nutritive, reproductive and immune functions (Gould et al, ; Groussin et al, ; Hanning & Diaz‐Sanchez, ; Ley et al, ; Turner, James, & Poole, ). As hosts vary in the microbiomes they harbour, an associated functionally important phenotypic variation exists within host populations (Falony et al, ; Ferrari & Vavre, ; Jaenike, ; Oliver, Russell, Moran, & Hunter, ; Scarborough, Ferrari, & Godfray, ).…”

Section: Introductionmentioning

confidence: 99%

Microbial community structure reveals instability of nutritional symbiosis during the evolutionary radiation of Amblyomma ticks

et al. 2020

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Mutualistic interactions with microbes have facilitated the adaptation of major eukaryotic lineages to restricted diet niches. Hence, ticks with their strictly blood‐feeding lifestyle are associated with intracellular bacterial symbionts through an essential B vitamin supplementation. In this study, examination of bacterial diversity in 25 tick species of the genus Amblyomma showed that three intracellular bacteria, Coxiella‐like endosymbionts (LE), Francisella‐LE and Rickettsia, are remarkably common. No other bacterium is as uniformly present in Amblyomma ticks. Almost all Amblyomma species were found to harbour a nutritive obligate symbiont, Coxiella‐LE or Francisella‐LE, that is able to synthesize B vitamins. However, despite the co‐evolved and obligate nature of these mutualistic interactions, the structure of microbiomes does not mirror the Amblyomma phylogeny, with a clear exclusion pattern between Coxiella‐LE and Francisella‐LE across tick species. Coxiella‐LE, but not Francisella‐LE, form evolutionarily stable associations with ticks, commonly leading to co‐cladogenesis. We further found evidence for symbiont replacements during the radiation of Amblyomma, with recent, and probably ongoing, invasions by Francisella‐LE and subsequent replacements of ancestral Coxiella‐LE through transient co‐infections. Nutritional symbiosis in Amblyomma ticks is thus not a stable evolutionary state, but instead arises from conflicting origins between unrelated but competing symbionts with similar metabolic capabilities.

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Microbiome interactions shape host fitness

Cited by 461 publications

References 40 publications

The microbiota influences the Drosophila melanogaster life history strategy

The microbiota influences the Drosophila melanogaster life history strategy

Gut microbiota in ulcerative colitis: insights on pathogenesis and treatment

Microbial community structure reveals instability of nutritional symbiosis during the evolutionary radiation of Amblyomma ticks

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