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Multi-Omics Analysis Reveals a Correlation Between the Host Multi-omics analysis reveals a correlation between the host phylogeny, gut microbiota and metabolite profiles in cyprinid fishes Tongtong Li, Meng Long, Huan Li, Francois Joel Gatesoupe, Xujie Zhang, Qianqian Zhang, Dongyue Feng, Aihua Li To cite this version: Tongtong Li, Meng Long, Huan Li, Francois Joel Gatesoupe, Xujie Zhang, et al.. Multi-omics analysis reveals a correlation between the host phylogeny, gut microbiota and metabolite profiles in cyprinid fishes. Frontiers in Microbiology, Frontiers Media, 2017, 8, 10.3389/fmicb.2017.00454. hal-01605404 HAL Id: hal-01605404 https://hal.archives-ouvertes.fr/hal-01605404 Submitted on 26 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License fmicb-08-00454 March 15, 2017 Time: 16:5 # 1 ORIGINAL RESEARCH published: 17 March 2017 doi: 10.3389/fmicb.2017.00454 Multi-Omics Analysis Reveals a Correlation between the Host Phylogeny, Gut Microbiota and Metabolite Profiles in Cyprinid Fishes Tongtong Li1,2†, Meng Long1†, Huan Li2, François-Joël Gatesoupe3, Xujie Zhang4, Qianqian Zhang1,5, Dongyue Feng6* and Aihua Li1,5* 1 State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China, 2 Key Laboratory of Environmental and Applied Microbiology, and Environmental Microbiology Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China, 3 Nutrition, Métabolisme et Aquaculture, Institut National de la Recherche Agronomique, University of Pau and Pays de l’Adour, Saint-Pée-sur-Nivelle, France, 4 College of Fisheries and Life Science, Shanghai Ocean University, Shanghai, China, Edited by: 5 Freshwater Aquaculture Collaborative Innovation Center of Hubei Province, Huazhong Agricultural University, Wuhan, Malka Halpern, China, 6 National Fisheries Technical Extension Center, Ministry of Agriculture, Beijing, China University of Haifa, Israel Reviewed by: David William Waite, Gut microbiota play key roles in host nutrition and metabolism. However, little is University of Queensland, Australia known about the relationship between host genetics, gut microbiota and metabolic Renee Maxine Petri, profiles. Here, we used high-throughput sequencing and gas chromatography/mass Veterinärmedizinische Universität, Austria spectrometry approaches to characterize the microbiota composition and the Frank O’Neill Aylward, metabolite profiles in the gut of five cyprinid fish species with three different feeding Center for Microbial Oceanography: Research and Education (C-MORE), habits raised under identical husbandry conditions. Our results showed that host USA species and feeding habits significantly affect not only gut microbiota composition *Correspondence: but also metabolite profiles (ANOSIM, p ≤ 0.05). Mantel test demonstrated that host Dongyue Feng phylogeny, gut microbiota, and metabolite profiles were significantly related to each [email protected] Aihua Li other (p ≤ 0.05). Additionally, the carps with the same feeding habits had more [email protected] similarity in gut microbiota composition and metabolite profiles. Various metabolites †These authors have contributed were correlated positively with bacterial taxa involved in food degradation. Our results equally to this work. shed new light on the microbiome and metabolite profiles in the gut content of cyprinid Specialty section: fishes, and highlighted the correlations between host genotype, fish gut microbiome and This article was submitted to putative functions, and gut metabolite profiles. Microbial Symbioses, a section of the journal Keywords: correlation, host phylogeny, gut microbiota, metabolite profiles, cyprinid fishes Frontiers in Microbiology Received: 16 December 2016 Accepted: 03 March 2017 INTRODUCTION Published: 17 March 2017 Citation: Vertebrates harbor vast and complex microbial communities that colonize their gastrointestinal Li T, Long M, Li H, Gatesoupe F-J, tracts (Walter et al., 2011). As a result of this intimate relationship, the gut microbiome has become Zhang X, Zhang Q, Feng D and Li A an integral part of the digestive system. The gut microbiota strongly influences fish health by (2017) Multi-Omics Analysis Reveals stimulating the development of the intestinal epithelium and the immune system, and impeding a Correlation between the Host pathogenic microorganisms to colonize the intestinal tract (Sugita et al., 1991; Flint et al., 2008; Phylogeny, Gut Microbiota and Metabolite Profiles in Cyprinid Ley et al., 2008b; Roeselers et al., 2011; Li T. et al., 2016). In the gastrointestinal tract, commensal Fishes. Front. Microbiol. 8:454. bacteria can synthesize essential amino acids, vitamins and short-chain fatty acids (SCFAs), doi: 10.3389/fmicb.2017.00454 and contribute to feed efficiency, especially by degrading indigestible plant polysaccharides Frontiers in Microbiology| www.frontiersin.org 1 March 2017| Volume 8| Article 454 fmicb-08-00454 March 15, 2017 Time: 16:5 # 2 Li et al. Genotype, Microbiota and Metabolite Related (Gill et al., 2006). Therefore, gut content and feces contain small performed here in on fish gut samples provided insights into the molecules that are considered to result from co-metabolism or relationship between microbial populations and metabolites. metabolic exchanges between microbes and host cells (Chen et al., The polyculture of carps with different feeding habits is a 2012). traditional method to optimize the use of trophic resources The composition of gut microbial communities is shaped by in ponds (Li et al., 2015). In the present study, the intestinal various internal and external factors, such as host genotype, diet, microbial community structure and global metabolite profiles of lifestyle, and surrounding environment (e.g., water temperature, five cyprinid fish species cohabitated in the same environment salinity) (Nayak, 2010; Sullam et al., 2012). Previous studies were investigated: herbivorous grass carp (Ctenopharyngodon of mammalian species revealed that their gut microbiota idellus, HG) and blunt snout bream (Megalobrama amblycephala, clustered according to diet rather than host phylogeny (Ley HB); omnivorous crucian carp (Carassius auratus, OC); et al., 2008a; Muegge et al., 2011). It was also shown that filter-feeding silver carp (Hypophthalmichthys molitrix, FS) identical twins had still significant differences in their gut and bighead carp (Hypophthalmichthys nobilis, FB). These five microbiota, although they shared much higher similarity between freshwater fishes are the major carps in Chinese aquaculture gut microbiota structures than genetically unrelated married and widely cultivated for food. In 2012, the production of these couples (Zoetendal et al., 2001). In addition, some scientists species reached 14.48 million tons in China, accounting for about demonstrated that the phylogenetic relationships of hominids 62.02% of the total freshwater-cultured fish annual output (MoA, were completely consistent with those of gut microbiota 2012). Furthermore, understanding the microbial community (Ochman et al., 2010; Moeller et al., 2014). During evolution, and metabolite profile in the gut of these fish species can provide changes in the composition of gut microbiota may lead to useful information to improve health and productivity of these shifts in its functions, which may finally influence host nutrition commercially valuable freshwater species. and environmental adaptability (Amato, 2013). Comparative To date, many studies focused on fish gastrointestinal analysis among various hosts and their microbiota revealed microbiota, and such studies only concentrated on some factors that both diet and host phylogeny have driven the evolution (e.g., diet, feed habits, and genotype of host) that may affect fish of gut microbiota (Ley et al., 2008a). However, the main gastrointestinal microbiota (Wu et al., 2012; Li et al., 2013, 2015; driving factor remains controversial. Thus, identifying shifts Ye et al., 2013). Little is known about the relationship among host in gut microbiota composition and diversity over evolutionary evolutionary distance, gut microbiota and metabolic profiles in timescales will be crucial to understanding how gut microbiota cyprinid fishes. Here, we investigated two key questions. First, of cyprinid fishes is involved in evolution and environmental do host genotype, gut microbiota and gut metabolic profiles adaptation. correlate between them? Secondly, what is the relationship The concept of metabonomics was first defined as “the between dominant microbes and key metabolic products in the quantitative measurement of the dynamic multiparametric fish guts? metabolic response of living systems to pathophysiological stimuli or genetic modification” (Nicholson et al., 1999; Nicholson and Wilson, 2003). Nowadays, metabonomics MATERIALS AND METHODS provides a systematic approach to characterize the metabolic phenotype, which results from a coordinated physiological Sample Collection and Pyrosequencing response to various intrinsic
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