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Worms Need Microbes Too: Microbiota, Health and Aging in Caenorhabditis Elegans

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Worms Need Microbes Too: Microbiota, Health and Aging in Caenorhabditis Elegans Bridge the Gap OPEN The C. elegans–microbe holobiont ACCESS Worms need microbes too: microbiota, health and aging in Caenorhabditis elegans Filipe Cabreiro*, David Gems Keywords: aging; C. elegans; metformin; microbiota; type-2 diabetes DOI 10.1002/emmm.201100972 Received April 09, 2013 / Revised June 07, 2013 / Accepted June 12, 2013 Introduction Many animal species live in close association with commensal and symbiotic microbes (microbiota). Recent studies have revealed that the status of gastrointestinal tract Animals and plants rarely live in microbiota can influence nutrition-related syndromes such as obesity and type-2 isolation but rather exist in intimate association with other species — par- diabetes, and perhaps aging. These morbidities have a profound impact in terms of ticularly microorganisms. The nature of individual suffering, and are an increasing economic burden to modern societies. Several host–microbe interactions is defined theories have been proposed for the influence of microbiota on host metabolism, but according to which participant experi- these largely remain to be proven. In this article we discuss how microbiota may be fi ences bene t or harm (Rosenberg & manipulated (via pharmacology, diet, or gene manipulation) in order to alter ‐ Zilber Rosenberg, 2011). For example, metabolism, immunity, health and aging in the host. The nematode Caenorhabditis host benefit with harm to the microbe elegans in combination with one microbial species is an excellent, defined model system occurs in a host–predator relationship, while host harm with microbe benefit to investigate the mechanisms of host–microbiota interactions, particularly given the occurs in host–pathogen relationships. combined power of worm and microbial genetics. We also discuss the multifaceted More characteristic of the symbiotic nature of the worm–microbe relationship, which likely encompasses predation, relationship between host and intestinal commensalism, pathogenicity and necromeny. microbiota is commensalism, where there is benefit to only one partner of this interaction, and mutualism, where there is benefit to both. 2006) — is thus involved in many metabolic processes with In mammals, host–microbe symbiotic interactions mainly important consequences to host physiology and in the modula- occur along mucosal surfaces, with the most important one tion of metabolic phenotypes. Consistent with this, sequence being the intestinal mucosa. The intestine harbours a vast analysis shows that the microbiome is importantly enriched in population of symbiotic microbes that outnumber host somatic genes encoding metabolic activities such as metabolism of cells by 10‐fold and are capable of performing varied metabolic xenobiotic compounds, amino acids and carbohydrates (Greiner and protective functions. Along the intestinal tract, bi‐directional & Backhed, 2011). Importantly, the microbiota contributes to the host–microbiota exchanges occur with mutual benefits to both fitness of the host by influencing development (Rawls organisms. Indeed, 10% of the metabolites in the mammalian et al, 2004), reproduction (Shimizu et al, 1998), metabolism blood flow are of bacterial origin (Wikoff et al, 2009). For (Cani & Delzenne, 2009; Nicholson et al, 2012), immunity (Kau instance, bacteria in the gut are capable of synthesizing and et al, 2011) and lifespan (Ottaviani et al, 2011). excreting vitamins, which can be absorbed by the host. The gut Gut microbiota status is also a determinant of health in the microbiota also plays an important role in catabolizing dietary host. Consequently, human health may be affected by factors fibre for human nutrition (Nicholson et al, 2012). The microbiota that alter microbiota, e.g. dietary changes and antibiotic usage, — referred to as “the forgotten organ” (O’Hara & Shanahan, which may reduce microbiota complexity (Maurice et al, 2013; Muegge et al, 2011). This has led to concern that disruption of microbiota could be contributing to conditions such as obesity, Institute of Healthy Ageing, and Research Department of Genetics, Evolution fl and Environment, University College London, London, UK diabetes, metabolic syndrome, autoimmune disorders, in am- *Corresponding author: Tel: þ44 207 679 2244; Fax: þ44 207 679 7096; matory bowel disease, cancer and aging (Cho & Blaser, 2012; E-mail: [email protected] Claesson et al, 2012). Thus, it is important to try to understand ß 2013 The Authors. Published by John Wiley and Sons, Ltd on behalf of EMBO. This is an open access article under the terms of the Creative Commons Attribution License (CC BY 3.0), which permits use, distribution and reproduction in any medium, provided the original work is properly cited. EMBO Mol Med (2013) 5, 1–11 1 Bridge the Gap www.embomolmed.org The C. elegans–microbe holobiont how these microbial communities determine human health reproduction (Brenner, 1974). In terms of its general suitability status, including healthy aging. as a model organism, these include the transparency of its body wall, which allow the internal organs, fat depots and age‐related pathology to be viewed; a very short lifespan (2– C. elegans as a model for host–microbiota 3 weeks); and excellent genetics, including a sequenced and interactions fully annotated genome, and availability of mutants and reagents for gene knock out. Moreover, fluorescently tagged The suspected role of host–microbiota interactions in human bacteria may be readily visualized within the transparent body disease is largely derived from observational studies, and it is of C. elegans providing easy assessment of gut colonization (Sifri often difficult to establish whether changes in microbiota are et al, 2005). cause or effect of their associated pathologies. The use of mouse In terms of suitability for host–microbiota studies, the models offers one solution, but the complexity of mouse intestine is the largest somatic organ in the worm, and it is microbiota presents a challenge, and mouse costs are another typically full of microbes (Felix & Duveau, 2012; Garigan impediment (Claesson et al, 2012). et al, 2002; McGee et al, 2011). The C. elegans intestine is a non‐ C. elegans has proven to be an excellent model for the study of renewable 20‐cell monolayer arranged to form a tube with a many central processes in biology, including energy metabolism central lumen (Brenner, 1974). The intestinal cells have a brush (Jones & Ashrafi, 2009), immunity (Schulenburg et al, 2004) and border on their apical side, comprising finger‐like microvilli aging (Kenyon, 2010). Could the worm also serve as a model attached to a terminal web of actin and intermediate filaments to understand how microbiota affect host physiology in the (Troemel et al, 2008). Functionally, and as in humans, the context of disease and aging? Several features of C. elegans intestine constitutes a first line of defence against a potential make it well‐equipped for such a role. C. elegans are easily harmful environment (e.g. pathogens; Ewbank & Zugasti, 2011; maintained monoxenically (i.e. with one bacterial species) in Lievin‐Le Moal & Servin, 2006) but at the same time provide a laboratory conditions. Growth and maintenance of the bacterial means for nutrient extraction, storage and absorption, as well as food source is achieved through standard microbiology waste excretion. In addition, the intestine plays a major role in technique. Nematode growth medium agar, which has been organismal health and lifespan, and acts as a signalling centre aseptically poured into Petri plates supports growth of seeded influencing other tissues and modulated by bacterially derived bacteria which in turn supports C. elegans growth and cues (Rera et al, 2013). Glossary Mutualism A relationship between individuals of different species in which both Biotransformation species benefit from the interaction. Chemical alteration by an organism of a chemical compound. These can include nutrients, toxins, xenobiotics. Necromeny The behaviour of an organism that attaches itself to a host organism, Commensalism and then feeds upon its decomposing cadaver after death. From the medieval Latin com mensa or ‘sharing the same table’. Relationship between individuals of two species, in which one species Pathobiont obtains benefits from the other without either harming or benefiting Member species of the microbiota that under conditions of host and/or the latter. microbiota dyshomeostasis can cause pathology. Distinct from pathogen. Dietary restriction Probiotic Reduction of dietary intake without starvation, which reduces fertility Live organisms that when ingested confer health benefits to the host and increases lifespan in many animal species. Also known as caloric either by interacting directly with the host or through modulation of restriction. other members of the microbiota. Bacterial strains from the genera Lactobacillus and Bifidobacterium are candidate probiotics. Dysbiosis State of microbial imbalance in the gut leading to host Symbiont dyshomeostasis. An organism in a mutually beneficial relationship with another. Gut microbiota Symbiosis The collective community of microbes inhabiting a host gastrointes- Close and long-term beneficial interaction between two species. tinal tract. In contrast to worms in the wild, nematodes in the laboratory are usually raised in the presence of a single bacterial Type‐2 diabetes strain. Pandemic disorder characterized by high blood glucose in the context of relative insulin deficiency and insulin resistance. About 6% of the Holobiont world population suffers from
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