Interspecies Systems Biology Uncovers Metabolites Affecting C. elegans Gene Expression and Life History Traits

Watson, Emma; MacNeil, Lesley T.; Ritter, Ashlyn D.; Yılmaz, L. Şafak; Rosebrock, Adam P.; Caudy, Amy A.; Walhout, Albertha J.M.

doi:10.1016/j.cell.2014.02.036

Cited by 59 publications

(94 citation statements)

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“…To survive challenging environments with fluctuating nutrient resources, animals have acquired the ability to evaluate food quality, which may lead to avoidance of food lacking certain essential nutrients or containing toxic molecules, and to alterations in developmental and metabolic programs (Bargmann, 2006; Bjordal et al, 2014; Chi et al, 2016; Chng et al, 2014; Ha et al, 2010; Iwatsuki and Torii, 2012; Kniazeva et al, 2015; Melo and Ruvkun, 2012; Tang and Han, 2017; Watson et al, 2014). Besides neuronal sensory systems that permit rapid feeding decision, food quality is also evaluated by the intestine-initiated systems that may be more sensitive in detecting the deficiency of certain types of nutrients including micronutrients and are capable of dictating changes in cellular/developmental programs as well as food uptake and seeking behaviors.…”

Section: Introductionmentioning

confidence: 99%

A vitamin-B2-sensing mechanism that regulates gut protease activity to impact animal’s food behavior and growth

Kniazeva

Han

2017

eLife

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To survive challenging environments, animals acquired the ability to evaluate food quality in the intestine and respond to nutrient deficiencies with changes in food-response behavior, metabolism and development. However, the regulatory mechanisms underlying intestinal sensing of specific nutrients, especially micronutrients such as vitamins, and the connections to downstream physiological responses in animals remain underexplored. We have established a system to analyze the intestinal response to vitamin B2 (VB2) deficiency in Caenorhabditis elegans, and demonstrated that VB2 level critically impacts food uptake and foraging behavior by regulating specific protease gene expression and intestinal protease activity. We show that this impact is mediated by TORC1 signaling through reading the FAD-dependent ATP level. Thus, our study in live animals uncovers a VB2-sensing/response pathway that regulates food-uptake, a mechanism by which a common signaling pathway translates a specific nutrient signal into physiological activities, and the importance of gut microbiota in supplying micronutrients to animals.DOI: http://dx.doi.org/10.7554/eLife.26243.001

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Section: Introductionmentioning

confidence: 99%

A vitamin-B2-sensing mechanism that regulates gut protease activity to impact animal’s food behavior and growth

Kniazeva

Han

2017

eLife

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“…E. coli is unable to synthesize vitamin B12 and instead scavenges exogenous B12 via a siderophore complex dependent on tonB [53]. This pathway has been shown to be vital for the uptake of B12 by C. elegans; a tonB mutant induces the expression of acdh-1p::GFP in C. elegans, (GFP under the control of the acyl-CoA dehydrogenase promoter) a dietary sensor of B12 deficiency [54], indicating that C. elegans is unable to uptake sufficient B12 directly from the growth media. E. coli therefore acts as a conduit for the provision of bioavailable B12 to C. elegans.…”

Section: E Coli Acts As a Conduit For Vitamin B12 Uptakementioning

confidence: 99%

“…E. coli therefore acts as a conduit for the provision of bioavailable B12 to C. elegans. The importance of this bacterial route is questioned, as expression of acdh-1p::GFP on E. coli was found to be suppressed with supplementation of B12 on both live and UV-killed bacteria [54]. The reason for this discrepancy is perhaps due to the increased bioavailability of B12 in a preparation of a B12 supplement compared with B12 present in trace amounts in the growth media.…”

Section: E Coli Acts As a Conduit For Vitamin B12 Uptakementioning

confidence: 99%

Bacteria increase host micronutrient availability: mechanisms revealed by studies in C. elegans

Maynard

Weinkove

2020

Genes Nutr

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Micronutrients cannot be synthesized by humans and are obtained from three different sources: diet, gut microbiota, and oral supplements. The microbiota generates significant quantities of micronutrients, but the contribution of these compounds to total uptake is unclear. The role of bacteria in the synthesis and uptake of micronutrients and supplements is widely unexplored and may have important implications for human health. The efficacy and safety of several micronutrient supplements, including folic acid, have been questioned due to some evidence of adverse effects on health. The use of the simplified animal-microbe model, Caenorhabditis elegans, and its bacterial food source, Escherichia coli, provides a controllable system to explore the underlying mechanisms by which bacterial metabolism impacts host micronutrient status. These studies have revealed mechanisms by which bacteria may increase the bioavailability of folic acid, B12, and iron. These routes of uptake interact with bacterial metabolism, with the potential to increase bacterial pathogenesis, and thus may be both beneficial and detrimental to host health.

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“…This assessment is in general agreement with previous work. For example, a strain of the soil bacterium Comamonas was shown to provide vitamin B12 to the worm, which in turn influences development and fertility through the methionine/SAdenosylmethionine cycle while it also processes propionic acid, thereby removing its toxic effects (Watson et al 2014(Watson et al , 2016 . Interestingly, the two CeMbio members MYb11 and MYb71, usually enriched in the C. elegans microbiome (Dirksen et al 2016;Zhang et al 2017;Zimmermann et al 2020a;Johnke et al 2020) ; see also below), also possess the pathways for vitamin B12 production (Zimmermann et al 2020a) and could thus influence similar C. elegans characteristics as the Comamonas strain.…”

Section: Whole Genome Sequences Reveal Diverse Metabolic Competences mentioning

confidence: 99%

CeMbio - TheC. elegansmicrobiome resource

Dirksen¹,

Assié

Zimmermann

et al. 2020

Preprint

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The study of microbiomes by sequencing has revealed a plethora of correlations between microbial community composition and various life-history characteristics of the corresponding host species. However, inferring causation from correlation is often hampered by the sheer compositional complexity of microbiomes, even in simple organisms. Synthetic communities offer an effective approach to infer cause-effect relationships in host-microbiome systems. Yet the available communities suffer from several drawbacks, such as artificial (thus non-natural) choice of microbes, microbe-host mismatch (e.g. human microbes in gnotobiotic mice), or hosts lacking genetic tractability. Here we introduce CeMbio, a simplified natural Caenorhabditis elegans microbiota derived from our previous meta-analysis of the natural microbiome of this nematode. The CeMbio resource is amenable to all strengths of the C. elegans model system, strains included are readily culturable, they all colonize the worm gut individually, and comprise a robust community that distinctly affects nematode life-history. Several tools have additionally been developed for the CeMbio strains, including diagnostic PCR primers, completely sequenced genomes, and metabolic network models. With CeMbio, we provide a versatile resource and toolbox for the in-depth dissection of naturally relevant host-microbiome interactions in C. elegans .Pseudomonadaceae , and Xanthomonodaceae ) and Bacteroidetes ( Sphingobacteriaceae , Weeksellaceae , Flavobacteriaceae ) (Zhang et al. 2017) .Here we establish a publicly available and well-defined model microbiome for use in C. elegans (CeMbio). This set is composed of 12 bacteria from 9 different families that represent the core microbiome of C. elegans based on analyses and empirical studies of intestinal colonization.These bacterial strains are presented with fully sequenced and annotated genomes, metabolic network reconstructions, and robust protocols for their use in C. elegans studies and beyond. All of the bacteria effectively colonize the C. elegans gut both alone and as a community, which can impact on the growth and development of the host. The CeMbio community has broad application to any aspect of C. elegans biology from aging to pathogenesis, development to neurobiology, and any aspect of physiology where a more natural environment is desired.Ultimately, pairing of this well-defined microbiome and highly-tractable host is envisioned to complement other systems (e.g., (Fraune and Bosch 2010;Brugiroux et al. 2016;Douglas 2019) ) in advancing understanding of the mechanisms of microbiome impact on host health and disease.

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Interspecies Systems Biology Uncovers Metabolites Affecting C. elegans Gene Expression and Life History Traits

Cited by 59 publications

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A vitamin-B2-sensing mechanism that regulates gut protease activity to impact animal’s food behavior and growth

A vitamin-B2-sensing mechanism that regulates gut protease activity to impact animal’s food behavior and growth

Bacteria increase host micronutrient availability: mechanisms revealed by studies in C. elegans

CeMbio - TheC. elegansmicrobiome resource

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