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Ecological Robustness of the Gut Microbiota in Response to Ingestion Ecological robustness of the gut microbiota in response to ingestion of transient food-borne microbes Chenhong Zhang, Muriel Derrien, Florence Levenez, Rémi Brazeilles, Sonia A. Ballal, Jason Kim, Marie-Christine Degivry, Gaëlle Quéré, Peggy Garault, Johan E. T. van Hylckama Vlieg, et al. To cite this version: Chenhong Zhang, Muriel Derrien, Florence Levenez, Rémi Brazeilles, Sonia A. Ballal, et al.. Eco- logical robustness of the gut microbiota in response to ingestion of transient food-borne microbes. ISME Journal, Nature Publishing Group, 2016, 10 (9), pp.2235-2245. 10.1038/ismej.2016.13. hal- 01604968 HAL Id: hal-01604968 https://hal.archives-ouvertes.fr/hal-01604968 Submitted on 28 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. The ISME Journal (2016) 10, 2235–2245 OPEN © 2016 International Society for Microbial Ecology All rights reserved 1751-7362/16 www.nature.com/ismej ORIGINAL ARTICLE Ecological robustness of the gut microbiota in response to ingestion of transient food-borne microbes Chenhong Zhang1, Muriel Derrien2, Florence Levenez1, Rémi Brazeilles2, Sonia A Ballal3, Jason Kim3, Marie-Christine Degivry2, Gaëlle Quéré2, Peggy Garault2, Johan ET van Hylckama Vlieg2,4, Wendy S Garrett3, Joël Doré1,5 and Patrick Veiga2,3,5 1Metagenopolis, Institut National de la Recherche Agronomique, Jouy-en-Josas, France; 2Life Science, Danone Nutricia Research, Palaiseau, France and 3Harvard T. H. Chan School of Public Health, Boston, MA, USA Resident gut microbes co-exist with transient bacteria to form the gut microbiota. Despite increasing evidence suggesting a role for transient microbes on gut microbiota function, the interplay between resident and transient members of this microbial community is poorly defined. We aimed to determine the extent to which a host’s autochthonous gut microbiota influences niche permissivity to transient bacteria using a fermented milk product (FMP) as a vehicle for five food-borne bacterial strains. Using conventional and gnotobiotic rats and gut microbiome analyses (16S rRNA genes pyrosequencing and reverse transcription qPCR), we demonstrated that the clearance kinetics of one FMP bacterium, Lactococcus lactis CNCM I-1631, were dependent on the structure of the resident gut microbiota. Susceptibility of the resident gut microbiota to modulation by FMP intervention correlated with increased persistence of L. lactis. We also observed gut microbiome configurations that were associated with altered stability upon exposure to transient bacteria. Our study supports the concept that allochthonous bacteria have transient and subject-specific effects on the gut microbiome that can be leveraged to re-engineer the gut microbiome and improve dysbiosis-related diseases. The ISME Journal (2016) 10, 2235–2245; doi:10.1038/ismej.2016.13; published online 8 March 2016 Introduction et al., 2013; Deriu et al., 2013; Laval et al., 2015; Martin et al., 2015). One of the many traits ascribed Mammals are holobionts that host microbial com- to the autochthonous (that is, resident) gut micro- munities of astounding density and complexity biota is its ability to prevent colonization by within their gastrointestinal (GI) tracts. Microorgan- allochthonous (that is, exogenous) bacteria, espe- isms from maternal and environmental microbiomes cially pathogens. This function of the microbial rapidly colonize the GI tract of the newborn, and a ecosystem is known as ‘colonization resistance’ or stable microbial ecosystem develops within the first ‘the barrier effect’ (van der Waaij et al., 1971). three years of life (Koenig et al., 2011). This Colonization resistance has been well-established microbial stability is then continuously challenged with respect to Escherichia coli, Clostridium difficile by daily ingestion of environmental bacteria origi- and Salmonella spp. (Que and Hentges 1985; Wilson nating from sources such as diet (van Hylckama et al., 1986; Vollaard et al., 1990; Stecher et al., 2005) Vlieg et al., 2011), indoor environments (Lax et al., and has been linked to certain features of the gut 2014), human co-inhabitants (Song et al., 2013) and, microbiota, for example, community complexity as more recently, by symbionts used to restore a well as the presence of specific taxa (de La perturbed microbiota (Reeves et al., 2012; Atarashi Cochetiere et al., 2010; Manges et al., 2010; Stecher et al., 2010; Rousseau et al., 2011). Bacteria in foodstuffs are a major source of Correspondence: J Doré, Institut National de la Recherche allochthonous bacteria, ranging from 104 to 109 Agronomique, Jouy-en-Josas, France. colony-forming units per gram of food with fermen- E-mail: [email protected] or P Veiga, Life Science, Danone Nutricia Research, Palaiseau ted foods having the highest viable bacterial counts 91120, France. (Lang et al., 2014). These food-borne bacteria can E-mail: [email protected] temporarily integrate into the gut microbiome and 4Present address: Chr. Hansen, Boege Allé 10-12, DK-2970, constitute what can be called the transient micro- Hoersholm Denmark. 5Co-senior authors. biome (McNulty et al., 2011; David et al., 2014; Received 23 June 2015; revised 18 December 2016; accepted Veiga et al., 2014; Eloe-Fadrosh et al., 2015). 8 January 2016; published online 8 March 2016 Emerging evidence suggests a significant role of Gut microbiota response to food-borne bacteria C Zhang et al 2236 transient food-borne bacteria on the overall gut specific pathogen-free animal facility, and fed a microbiota community structure and function standard autoclaved chow diet (ref. R03, SAFE, (McNulty et al., 2011; Veiga et al., 2014; Derrien Augy, France) ad libitum. After adaptation and and van Hylckama Vlieg 2015; Unno et al., 2015). 15 days of run-in, the rats were gavaged with the In the present study, we examined if a host’s FMP (0.5 ml per day) for 15 days (Day 1–15). During autochthonous gut microbiota influences niche the last 5 days of the gavage period, Geobacillus permissivity (that is, colonization resistance) for stearothermophilus spores (Merck, Darmstadt, transient bacteria administered in a fermented milk Germany) were added to the FMP as a GI transit product (FMP) containing a consortium of five marker (107 day per rat). Spores collected from fecal strains: Bifidobacterium animalis subsp. lactis samples were germinated at 65 °C in G-spore CNCM I-2494, Lactococcus lactis subsp. lactis medium (Drouault et al., 2002). The 15 days after CNCM I-1631 Lactobacillus delbrueckii subsp. the FMP gavage served as a wash-out period (Day bulgaricus CNCM I-1632, L. delbrueckii subsp. 16–30). The feces of the rats were collected during bulgaricus CNCM I-1519 and Streptococcus thermo- the experimental period and the collection time philus CNCM I-1630. Following FMP administration points are shown in Figure 1a. to conventional rats, we observed that one subgroup of rats (hereafter called ‘resistant’) eliminated L. lactis CNCM I-1631 as fast as a GI transit RNA and DNA extraction − marker, whereas another subgroup (hereafter called The fecal samples were stored at 80 °C until RNA ‘permissive’) shed the strain over an additional and DNA extraction. The RNA was extracted by High 24–48 h. Gut microbiota analyses showed that Pure Isolation Kit (Roche, Branford, CT, USA) with resistant and permissive rats differed in their an improved protocol described previously (Tap abundance of Lachnospiraceae and that resistant et al., 2015). A frozen aliquot (200 mg) of each fecal μ rats had a microbiota less susceptible to FMP- sample was suspended in 250 l of guanidine μ induced changes compared with the permissive rats. thiocyanate, 0.1 M Tris (pH 7.5) and 40 lof10% Based on these findings, we re-analyzed the 16S N-lauroyl sarcosine, and DNA was extracted as ribosomal RNA (rRNA) amplicon survey data from previously described (Manichanh et al., 2006). the McNulty et al.'s, study (2011), which investi- RNA and DNA concentration and molecular weight gated the effects of a similar FMP on human gut were estimated using a nanodrop instrument microbiota (n=14), and observed similar patterns. (Thermo Scientific, Wilmington, DE, USA) and We then used fecal transplantation in germ-free rats agarose gel electrophoresis, respectively. to demonstrate that the resistant and permissive phenotypes were gut microbiota-dependent. Fecal quantitative reverse transcription PCR The bacterial culture used for standard curves, the primers and quantitative reverse transcription Materials and methods PCR system and protocol were described Study product previously (Veiga et al., 2010) (Supplementary The product was an FMP (Danone Research), Table S1). The quantity of each FMP strain was which contains the following strains: L. lactis subsp. normalized by the number of total bacteria. We lactis (strain I-1631 from the French National converted the number of detected molecules (RNA) Collection of Cultures of Microorganisms (CNCM), into cell equivalents. Paris, France), B. animalis subsp. lactis CNCM I-2494, L. delbrueckii subsp. bulgaricus CNCM I-1632, Pyrosequencing of the V3–V4 region of 16S rRNA genes L. delbrueckii subsp. bulgaricus CNCM I-1519 The PCR of the V3–V4 region of 16S rRNA genes and S. thermophilus CNCM I-1630. The FMP − and pyrosequencing was performed by Genoscreen contains ~ 108 colony-forming units L. lactis ml 1, − − (France, www.genoscreen.com) with GS-FLX B. lactis ml 1, L. bulgaricus ml 1 and 6 × 108 − platform (Roche). The following universal 16S rRNA S. thermophilus ml 1. The energy density of the − primers were used for the PCR reactions: V3F FMP was 6.0–7.2 kcal g 1 and the pH values were (TACGGRAGGCAGCAG, 343–357 E.
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