The DOI matches its Crossref record; 64 of the 64 references it cites were found in a registry or an index.
Experimental Evaluation of Host Adaptation of Lactobacillus reuteri to Different Vertebrate Species
Open accessAbstract
The species Lactobacillus reuteri has diversified into host-specific lineages, implying a long-term association with different vertebrates. Strains from rodent lineages show specific adaptations to mice, but the processes underlying the evolution of L. reuteri in other hosts remain unknown. We administered three standardized inocula composed of strains from different host-confined lineages to mice, pigs, chickens, and humans. The ecological performance of each strain in the gastrointestinal tract of each host was determined by typing random colonies recovered from fecal samples collected over five consecutive days postadministration. Results revealed that rodent strains were predominant in mice, confirming previous findings of host adaptation. In chickens, poultry strains of the lineage VI (poultry VI) and human isolates from the same lineage (human VI) were recovered at the highest and second highest rates, respectively. Interestingly, human VI strains were virtually undetected in human feces. These findings, together with ancestral state reconstructions, indicate poultry VI and human VI strains share an evolutionary history with chickens. Genomic analysis revealed that poultry VI strains possess a large and variable accessory genome, whereas human VI strains display low genetic diversity and possess genes encoding antibiotic resistance and capsular polysaccharide synthesis, which might have allowed temporal colonization of humans. Experiments in pigs and humans did not provide evidence of host adaptation of L. reuteri to these hosts. Overall, our findings demonstrate host adaptation of L. reuteri to rodents and chickens, supporting a joint evolution of this bacterial species with several vertebrate hosts, although questions remain about its natural history in humans and pigs. IMPORTANCE Gut microbes are often hypothesized to have coevolved with their vertebrate hosts. However, the evidence is sparse and the evolutionary mechanisms have not been identified. We developed and applied an experimental approach to determine host adaptation of L. reuteri to different hosts. Our findings confirmed adaptation to rodents and provided evidence of adaptation to poultry, suggesting that L. reuteri evolved via natural selection in different hosts. By complementing phylogenetic analyses with experimental evidence, this study provides novel information about the mechanisms driving host-microbe coevolution with vertebrates and serve as a basis to inform the application of L. reuteri as a probiotic for different host species.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The cited source says what the claim attributes to it.
In the citing paper
“For example, Clade VI strains of Lactobacillus reuteri exhibit elevated fitness in chickens even if isolated from humans.41”
From Gut microbiota drives structural variation of exogenous probiotics to enhance colonization (2025) · cites this paper as [41]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Hall, T. A. (1999) · Nucleic Acids Symposium Series · doi:10.14601/phytopathol_mediterr-14998u1.29 · Cited by 38,156
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing
Bankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M. V., Kulikov, A. S., Lesin, V. M., Nikolenko, S., Pham, S., Prjibelski, A. D., et al. (2012) · Journal of Computational Biology · doi:10.1089/cmb.2012.0021 · Cited by 26,312
A human gut microbial gene catalogue established by metagenomic sequencing
MetaHIT Consortium, Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., Nielsen, T., Pons, N., Levenez, F., et al. (2010) · Nature · doi:10.1038/nature08821 · Cited by 11,624
(2009) · Cited by 6,571
BEAST 2: a software platform for Bayesian evolutionary analysis
Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C.-H., Xie, D., Suchard, M. A., Rambaut, A., & Drummond, A. J. (2014) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003537 · Cited by 6,527
Vaginal microbiome of reproductive-age women
Ravel, J., Gajer, P., Abdo, Z., Schneider, G. M., Koenig, S. S. K., McCulle, S. L., Karlebach, S., Gorle, R., Russell, J., Tacket, C. O., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002611107 · Cited by 4,254
progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement
Darling, A. E., Mau, B., & Perna, N. T. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011147 · Cited by 3,848
Evolution of mammals and their gut microbes
Ley, R. E., Hamady, M., Lozupone, C., Turnbaugh, P. J., Ramey, R. R., Bircher, J. S., Schlegel, M. L., Tucker, T. A., Schrenzel, M. D., Knight, R., et al. (2008) · Science · doi:10.1126/science.1155725 · Cited by 3,747
Worlds within worlds: evolution of the vertebrate gut microbiota
Ley, R. E., Lozupone, C., Hamady, M., Knight, R. D., & Gordon, J. I. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1978 · Cited by 1,697
An ecological and evolutionary perspective on human–microbe mutualism and disease
Dethlefsen, L., McFall-Ngai, M., & Relman, D. A. (2007) · Nature · doi:10.1038/nature06245 · Cited by 1,660
PATRIC, the bacterial bioinformatics database and analysis resource
Wattam, A. R., Abraham, D., Dalay, O., Disz, T. L., Driscoll, T., Gabbard, J. L., Gillespie, J. J., Gough, R., Hix, D., Kenyon, R. W., et al. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt1099 · Cited by 1,258
Painter, J. A., Hoekstra, R. M., Ayers, T., Tauxe, R. V., Braden, C. R., Angulo, F. J., & Griffin, P. M. (2013) · Emerging Infectious Diseases · doi:10.3201/eid1903.111866 · Cited by 1,146 · cited 1×
“5 million cases per year of foodborne illnesses in the United States that arise from the transmission of pathogens from poultry, meat, and eggs (36).”
BackgroundYersinia pestis , the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis
Achtman, M., Zurth, K., Morelli, G., Torrea, G., Guiyoule, A., & Carniel, E. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.24.14043 · Cited by 1,126
Traces of Human Migrations in Helicobacter pylori Populations
Falush, D., Wirth, T., Linz, B., Pritchard, J. K., Stephens, M., Kidd, M. S., Blaser, M. J., Graham, D. Y., Vacher, S., Perez-Perez, G. I., et al. (2003) · Science · doi:10.1126/science.1080857 · Cited by 1,019
What are the consequences of the disappearing human microbiota?
Blaser, M. J., & Falkow, S. (2009) · Nature Reviews Microbiology · doi:10.1038/nrmicro2245 · Cited by 878
Culture-Independent Analysis of Gut Bacteria: the Pig Gastrointestinal Tract Microbiota Revisited
Leser, T. D., Amenuvor, J. Z., Jensen, T. K., Lindecrona, R. H., Boyé, M., & Møller, K. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.2.673-690.2002 · Cited by 868
Walter, J. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.00753-08 · Cited by 756
Self-citationA selective medium for the isolation and enumeration of oral and fecal lactobacilli
Rogosa, M., Mitchell, J. A., & Wiseman, R. F. (1951) · Journal of Bacteriology · doi:10.1128/jb.62.1.132-133.1951 · Cited by 653 · cited 1×
“To ensure selective cultivation from feces, an LRIM was devised based on the recipe of the Rogosa medium (54).”
MethodIntestinal colonization resistance
Lawley, T. D., & Walker, A. W. (2013) · Immunology · doi:10.1111/j.1365-2567.2012.03616.x · Cited by 610
STEVENS, C. E., & Hume, I. D. (1998) · Physiological Reviews · doi:10.1152/physrev.1998.78.2.393 · Cited by 579
Martínez, I., Stegen, J. C., Maldonado-Gómez, M. X., Eren, A. M., Siba, P. M., Greenhill, A. R., & Walter, J. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.03.049 · Cited by 576
Self-citationCospeciation of gut microbiota with hominids
Moeller, A. H., Caro‐Quintero, A., Mjungu, D. C., Georgiev, A. V., Lonsdorf, E. V., Muller, M. N., Pusey, A. E., Peeters, M., Hahn, B. H., & Ochman, H. (2016) · Science · doi:10.1126/science.aaf3951 · Cited by 576
Molecular Interactions between Bacterial Symbionts and Their Hosts
Dale, C., & Moran, N. A. (2006) · Cell · doi:10.1016/j.cell.2006.07.014 · Cited by 547
Diet shapes the gut microbiome of pigs during nursing and weaning
Frese, S. A., Parker, K., Calvert, C. C., & Mills, D. A. (2015) · Microbiome · doi:10.1186/s40168-015-0091-8 · Cited by 545
Self-citationThe Hologenome Concept: Helpful or Hollow?
Moran, N. A., & Sloan, D. B. (2015) · PLoS Biology · doi:10.1371/journal.pbio.1002311 · Cited by 533
Microbes Drive Evolution of Animals and Plants: the Hologenome Concept
ROSENBERG, E. B., & Zilber‐Rosenberg, I. (2016) · mBio · doi:10.1128/mbio.01395-15 · Cited by 525
Maldonado-Gómez, M. X., Martínez, I., Bottacini, F., O’Callaghan, A., Ventura, M., van Sinderen, D., Hillmann, B., Vangay, P., Knights, D., Hutkins, R. W., et al. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.09.001 · Cited by 517
Self-citationEvolutionary Relationships of Wild Hominids Recapitulated by Gut Microbial Communities
Ochman, H., Worobey, M., Kuo, C., Ndjango, J.-B. N., Peeters, M., Hahn, B. H., & Hugenholtz, P. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000546 · Cited by 511
Genomics and host specialization of honey bee and bumble bee gut symbionts
Kwong, W. K., Engel, P., Koch, H., & Moran, N. A. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1405838111 · Cited by 426
The Lactobacillus and Bifidobacterium microflora of the human intestine: composition and succession.
Reuter, G. (2001) · PubMed · Cited by 416
Jost, T., Lacroix, C., Braegger, C., & Chassard, C. (2013) · British Journal Of Nutrition · doi:10.1017/s0007114513000597 · Cited by 371
EDGAR 2.0: an enhanced software platform for comparative gene content analyses
Blom, J., Kreis, J., Spänig, S., Juhre, T., Bertelli, C., Ernst, C., & Goesmann, A. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw255 · Cited by 369
Self-citationEvolutionary transitions in bacterial symbiosis
Sachs, J. L., Skophammer, R. G., & Regus, J. U. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100304108 · Cited by 367
Moran, N. A. (2006) · Current Biology · doi:10.1016/j.cub.2006.09.019 · Cited by 358
Walter, J., Britton, R. A., & Roos, S. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000099107 · Cited by 341
Self-citationWhy bacteria matter in animal development and evolution
Fraune, S., & Bosch, T. C. G. (2010) · BioEssays · doi:10.1002/bies.200900192 · Cited by 321
The Evolution of Host Specialization in the Vertebrate Gut Symbiont Lactobacillus reuteri
Frese, S. A., Benson, A. K., Tannock, G. W., Loach, D. M., Kim, J., Zhang, M., Oh, P. L., Heng, N. C. K., Patil, P. B., Juge, N., et al. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1001314 · Cited by 312
Self-citationSiezen, R. J., Tzeneva, V. A., Castioni, A., Wels, M., Phan, H. T. K., Rademaker, J. L. W., Starrenburg, M. J. C., Kleerebezem, M., Douwe Molenaar, B., & Vlieg, J. E. T. V. H. (2009) · Environmental Microbiology · doi:10.1111/j.1462-2920.2009.02119.x · Cited by 293
Diversification of the gut symbiont Lactobacillus reuteri as a result of host-driven evolution
Oh, P. L., Benson, A. K., Peterson, D. A., Patil, P. B., Moriyama, E. N., Roos, S., & Walter, J. (2009) · The ISME Journal · doi:10.1038/ismej.2009.123 · Cited by 282
Self-citationMartino, M. E., Bayjanov, J. R., Caffrey, B. E., Wels, M., Joncour, P., Hughes, S., Gillet, B., Kleerebezem, M., van Hijum, S. A. F. T., & Leulier, F. (2016) · Environmental Microbiology · doi:10.1111/1462-2920.13455 · Cited by 264
Rosander, A., Connolly, E., & Roos, S. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.00991-08 · Cited by 239
Douillard, F. P., Ribbera, A., Kant, R., Pietilä, T. E., Järvinen, H. M., Messing, M., Randazzo, C. L., Paulin, L. G., Laine, P., Ritari, J., et al. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003683 · Cited by 238
Willis, L. M., & Whitfield, C. (2013) · Carbohydrate Research · doi:10.1016/j.carres.2013.05.007 · Cited by 233
On the origin of prokaryotic speciesPreprint
Doolittle, W. F., & Zhaxybayeva, O. (2009) · Genome Research · doi:10.1101/gr.086645.108 · Cited by 224
Bacterial Glycans: Key Mediators of Diverse Host Immune Responses
Comstock, L. E., & Kasper, D. L. (2006) · Cell · doi:10.1016/j.cell.2006.08.021 · Cited by 215
The integrated microbial genomes (IMG) system in 2007: data content and analysis tool extensions
Markowitz, V. M., Szeto, E., Palaniappan, K., Grechkin, Y., Chu, K., Chen, I.-M. A., Dubchak, I. L., Anderson, I., Lykidis, A., Mavromatis, K., et al. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm846 · Cited by 211
A single regulatory gene is sufficient to alter bacterial host range
Mandel, M. J., Wollenberg, M. S., Stabb, E. V., Visick, K. L., & Ruby, E. G. (2009) · Nature · doi:10.1038/nature07660 · Cited by 206
Martínez, I., Muller, C. E., & Walter, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069621 · Cited by 181
Self-citationSmokvina, T., Wels, M., Polka, J. U., Chervaux, C., Brisse, S., Boekhorst, J., Vlieg, J. E. T. V. H., & Siezen, R. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068731 · Cited by 162
Molecular Characterization of Host-Specific Biofilm Formation in a Vertebrate Gut Symbiont
Frese, S. A., MacKenzie, D. A., Peterson, D. A., Schmaltz, R. J., Fangman, T., Zhou, Y., Zhang, C. H., Benson, A. K., Cody, L. A., Mulholland, F., et al. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1004057 · Cited by 156
Self-citationInsights from genomic comparisons of genetically monomorphic bacterial pathogens
Achtman, M. (2012) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0303 · Cited by 131
Evolution of host specialization in gut microbes: the bee gut as a model
Kwong, W. K., & Moran, N. A. (2015) · Gut Microbes · doi:10.1080/19490976.2015.1047129 · Cited by 116
Proteins with GGDEF and EAL domains regulatePseudomonas putidabiofilm formation and dispersal
Gjermansen, M., Ragas, P. C., & Tolker‐Nielsen, T. (2006) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2006.00493.x · Cited by 107
Spinler, J. K., Sontakke, A., Hollister, E. B., Venable, S. F., Oh, P. L., Balderas, M. A., Saulnier, D. M. A., Mistretta, T., Devaraj, S., Walter, J., et al. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu137 · Cited by 106
Self-citationHilmi, H. T. A., Surakka, A., Apajalahti, J., & Saris, P. E. J. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.01128-07 · Cited by 98
The symbiont side of symbiosis: do microbes really benefit?
Garcia, J. R., & Gerardo, N. M. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00510 · Cited by 84
Pot, B., Felis, G. E., Bruyne, K. D., Tsakalidou, E., Papadimitriou, K., Leisner, J. J., & Vandamme, P. A. R. (2014) · Wiley eBooks · doi:10.1002/9781118655252.ch19 · Cited by 83
Frese, S. A., Hutkins, R. W., & Walter, J. (2012) · Advances in Microbiology · doi:10.4236/aim.2012.23051 · Cited by 68
Self-citationGnotobiotic pigs-derivation and rearing.
Miniats, O. P., & Jol, D. (1978) · PubMed · Cited by 64
Bongrand, C., Koch, E. J., Moriano‐Gutierrez, S., Cordero, O. X., McFall‐Ngai, M., Polz, M. F., & Ruby, E. G. (2016) · The ISME Journal · doi:10.1038/ismej.2016.69 · Cited by 62
Wollenberg, M. S., & Ruby, E. G. (2011) · The ISME Journal · doi:10.1038/ismej.2011.92 · Cited by 57
The pan-genome of Lactobacillus reuteri strains originating from the pig gastrointestinal tract
Wegmann, U., MacKenzie, D. A., Zheng, J., Goesmann, A., Roos, S., Swarbreck, D., Walter, J., Crossman, L. C., & Juge, N. (2015) · BMC Genomics · doi:10.1186/s12864-015-2216-7 · Cited by 49
Self-citationRattanaprasert, M., Roos, S., Hutkins, R. W., & Walter, J. (2014) · Journal of Functional Foods · doi:10.1016/j.jff.2014.05.017 · Cited by 44
Self-citationGoin, C. (2010) · Lincoln (University of Nebraska) · Cited by 4
Flagged first, then by citations
Research works printed but not linked: 2
- Tannock GW . 1992. The lactic microflora of pigs, mice and rats, p 21–48. InWoodBJB (ed), The lactic acid bacteria, vol 1. The lactic acid bacteria in health and disease. Springer US, Boston, MA.
- 10.1073/pnas.100261107 · DOI
Cited by
Sorted by citations
Zheng, J., Wittouck, S., Salvetti, E., Franz, C. M. A. P., Harris, H. M. B., Mattarelli, P., O’Toole, P. W., Pot, B., Vandamme, P., Walter, J., et al. (2020) · International Journal of Systematic and Evolutionary Microbiology · doi:10.1099/ijsem.0.004107 · Cited by 3,313
Self-citationLifestyles in transition: evolution and natural history of the genus Lactobacillus
Duar, R. M., Lin, X. B., Zheng, J., Martino, M. E., Grenier, T., Pérez-Muñoz, M. E., Leulier, F., Gänzle, M. G., & Walter, J. (2017) · FEMS Microbiology Reviews · doi:10.1093/femsre/fux030 · Cited by 567
Self-citationIntestinal Lactobacillus in health and disease, a driver or just along for the ride?
Heeney, D. D., Gareau, M. G., & Marco, M. L. (2017) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2017.08.004 · Cited by 367
The food-gut axis: lactic acid bacteria and their link to food, the gut microbiome and human health
De Filippis, F., Pasolli, E., & Ercolini, D. (2020) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuaa015 · Cited by 303
Gut microbiota–derived short‐chain fatty acids regulate group 3 innate lymphoid cells in HCC
Hu, C., Xu, B., Wang, X., Wan, W., Lu, J., Kong, D., Jin, Y., You, W., Sun, H., Mu, X., et al. (2022) · Hepatology · doi:10.1002/hep.32449 · Cited by 214
Metadata
- Authors
- Duar, R. M., Frese, S. A., Lin, X. B., Fernando, S. C., Burkey, T. E., Tasseva, G., Peterson, D. A., Blom, J., Wenzel, C. Q., Szymanski, C. M., & Walter, J.
- Affiliations
- University of Nebraska–Lincoln (US)
- University of Alberta (CA)
- Justus-Liebig-Universität Gießen (DE)
- ORCID
- Venue
- Applied and Environmental Microbiology
- Publisher
- American Society for Microbiology
- Published
- 2017-06-15
- Volume
- 83
- Issue
- 12
- ISSN
- 0099-2240 (ISSN-L)
- 1098-5336
- PMC
- PMC5452824
- OpenAlex
- W2604642477
- Cited by
- 104
- References
- 64
- Citations by year
- 2026: 9 · 2025: 15 · 2024: 9 · 2023: 13 · 2022: 12 · 2021: 6 · 2020: 17 · 2019: 8 · 2018: 10 · 2017: 5
- FWCI
- 12.31
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Applied and Environmental Microbiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- Lactobacillus reuteri, host adaptation, host-microbe coevolution, intestinal colonization, poultry strains, human strains, pigs, accessory genome, antibiotic resistance genes, capsular polysaccharide biosynthesis, probiotics, experimental infection
- MeSH terms
- Adaptation, Biological, Animals, Chickens, Biological Evolution, Humans, Phylogeny, Swine, Vertebrates, Gastrointestinal Tract, Mice, Limosilactobacillus reuteri, Host Specificity
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
