Functional Dynamics of the Gut Microbiome in Elderly People during Probiotic Consumption
Open accessAbstract
A mechanistic understanding of the purported health benefits conferred by consumption of probiotic bacteria has been limited by our knowledge of the resident gut microbiota and its interaction with the host. Here, we detail the impact of a single-organism probiotic, Lactobacillus rhamnosus GG ATCC 53103 (LGG), on the structure and functional dynamics (gene expression) of the gut microbiota in a study of 12 healthy individuals, 65 to 80 years old. The analysis revealed that while the overall community composition was stable as assessed by 16S rRNA profiling, the transcriptional response of the gut microbiota was modulated by probiotic treatment. Comparison of transcriptional profiles based on taxonomic composition yielded three distinct transcriptome groups that displayed considerable differences in functional dynamics. The transcriptional profile of LGG in vivo was remarkably concordant across study subjects despite the considerable interindividual nature of the gut microbiota. However, we identified genes involved in flagellar motility, chemotaxis, and adhesion from Bifidobacterium and the dominant butyrate producers Roseburia and Eubacterium whose expression was increased during probiotic consumption, suggesting that LGG may promote interactions between key constituents of the microbiota and the host epithelium. These results provide evidence for the discrete functional effects imparted by a specific single-organism probiotic and challenge the prevailing notion that probiotics substantially modify the resident microbiota within nondiseased individuals in an appreciable fashion. IMPORTANCE Probiotic bacteria have been used for over a century to promote digestive health. Many individuals report that probiotics alleviate a number of digestive issues, yet little evidence links how probiotic microbes influence human health. Here, we show how the resident microbes that inhabit the healthy human gut respond to a probiotic. The well-studied probiotic Lactobacillus rhamnosus GG ATCC 53103 (LGG) was administered in a clinical trial, and a suite of measurements of the resident microbes were taken to evaluate potential changes over the course of probiotic consumption. We found that LGG transiently enriches for functions to potentially promote anti-inflammatory pathways in the resident microbes.
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
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?
Data showing butyrate treatment protects against age-related muscle atrophy supports the idea that pre- and/or probiotic supplementation may prophylactically moderate aging muscle loss.
“data showing butyrate (associated with Bifidobacterium [72]) treatment to protect against age-related muscle atrophy [73] supports the idea that pre- and/or probiotic supplementation, which is shown to increase the abundance of Bifidobacterium and butyrate producers in older individuals [74, 75], may prophylactically moderate aging muscle loss.”
From Gut Microbiota Contribute to Age-Related Changes in Skeletal Muscle Size, Composition, and Function: Biological Basis for a Gut-Muscle Axis (2018) · cites this paper as [74]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364 · see citing works
QIIME allows analysis of high-throughput community sequencing data
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Peña, A. G., Goodrich, J. K., Gordon, J. I., et al. (2010) · Nature Methods · doi:10.1038/nmeth.f.303 · Cited by 34,887 · see citing works
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009) · Genome Biology · doi:10.1186/gb-2009-10-3-r25 · Cited by 21,849 · see citing works
HTSeq—a Python framework to work with high-throughput sequencing data
Anders, S., Pyl, P. T., & Huber, W. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btu638 · Cited by 21,464 · see citing works
Metagenomic biomarker discovery and explanation
Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W. S., & Huttenhower, C. (2011) · Genome Biology · doi:10.1186/gb-2011-12-6-r60 · Cited by 16,192 · see citing works
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
Stamatakis, A. (2006) · Bioinformatics · doi:10.1093/bioinformatics/btl446 · Cited by 15,582 · see citing works
UCHIME improves sensitivity and speed of chimera detection
Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., & Knight, R. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr381 · Cited by 15,114 · see citing works
Diet rapidly and reproducibly alters the human gut microbiome
David, L. A., Maurice, C. F., Carmody, R. N., Gootenberg, D. B., Button, J. E., Wolfe, B. E., Ling, A. V., Devlin, A. S., Varma, Y., Fischbach, M. A., et al. (2014) · Nature · doi:10.1038/nature12820 · Cited by 10,100 · see citing works
Fitting Linear Mixed-Effects Models Using lme4Preprint
Bates, D. M., Maechler, M., Bolker, B. M., & Walker, S. (2014) · arXiv (Cornell University) · doi:10.3929/ethz-b-000105397 · Cited by 9,435 · see citing works
A scaling normalization method for differential expression analysis of RNA-seq data
Robinson, M. D., & Oshlack, A. (2010) · Genome Biology · doi:10.1186/gb-2010-11-3-r25 · Cited by 7,876 · see citing works
Pruesse, E., Quast, C., Knittel, K., Fuchs, B. M., Ludwig, W., Peplies, J., & Glöckner, F. O. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm864 · Cited by 6,682 · see citing works
Diversity, stability and resilience of the human gut microbiota
Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K., & Knight, R. (2012) · Nature · doi:10.1038/nature11550 · Cited by 5,533 · see citing works
McCarthy, D. J., Chen, Y., & Smyth, G. K. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks042 · Cited by 5,195 · see citing works
The KEGG resource for deciphering the genome
Kanehisa, M. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkh063 · Cited by 5,121 · see citing works
McDonald, D. T., Price, M. N., Goodrich, J. K., Nawrocki, E. P., DeSantis, T. Z., Probst, A. J., Andersen, G. L., Knight, R. D., & Hugenholtz, P. (2011) · The ISME Journal · doi:10.1038/ismej.2011.139 · Cited by 5,010 · see citing works
PyNAST: a flexible tool for aligning sequences to a template alignment
Caporaso, J. G., Bittinger, K. L., Bushman, F. D., DeSantis, T. Z., Andersen, G. L., & Knight, R. D. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp636 · Cited by 3,374 · see citing works
Gut microbiota composition correlates with diet and health in the elderly
Claesson, M. J., Jeffery, I. B., Conde, S., Power, S. E., O’Connor, E. M., Cusack, S., Harris, H. M. B., Coakley, M., Lakshminarayanan, B., O’Sullivan, O., et al. (2012) · Nature · doi:10.1038/nature11319 · Cited by 3,314 · see citing works
Peng, Y., Leung, H. C. M., Yiu, S., & Chin, F. Y. L. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts174 · Cited by 2,997 · see citing works
Ab initio gene identification in metagenomic sequences
Zhu, W., Lomsadze, A., & Borodovsky, M. Y. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq275 · Cited by 1,793 · see citing works
Composition, variability, and temporal stability of the intestinal microbiota of the elderly
Claesson, M. J., Cusack, S., O'Sullivan, O., Greene-Diniz, R., de Weerd, H., Flannery, E., Marchesi, J. R., Falush, D., Dinan, T., Fitzgerald, G., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000097107 · Cited by 1,754 · see citing works
Through Ageing, and Beyond: Gut Microbiota and Inflammatory Status in Seniors and Centenarians
Biagi, E., Nylund, L., Candela, M., Ostan, R., Bucci, L., Pini, E., Nikkïla, J., Monti, D., Satokari, R., Franceschi, C., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010667 · Cited by 1,483 · see citing works
The Application of Ecological Theory Toward an Understanding of the Human Microbiome
Costello, E. K., Stagaman, K., Dethlefsen, L., Bohannan, B. J. M., & Relman, D. A. (2012) · Science · doi:10.1126/science.1224203 · Cited by 1,437 · see citing works
Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens
Lebeer, S., Vanderleyden, J., & De Keersmaecker, S. C. J. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2297 · Cited by 1,062 · see citing works
Genomic variation landscape of the human gut microbiome
Schloissnig, S., Arumugam, M., Sunagawa, S., Mitreva, M., Tap, J., Zhu, A., Waller, A., Mende, D. R., Kultima, J. R., Martin, J., et al. (2013) · Nature · doi:10.1038/nature11711 · Cited by 907 · see citing works
Rfam 11.0: 10 years of RNA families
Burge, S., Daub, J., Eberhardt, R. Y., Tate, J. G., Barquist, L., Nawrocki, E. P., Eddy, S. R., Gardner, P. P., & Bateman, A. G. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks1005 · Cited by 807 · see citing works
RNA Viral Community in Human Feces: Prevalence of Plant Pathogenic Viruses
Zhang, T., Breitbart, M., Lee, W. H., Run, J., Wei, C. L., Soh, S. W., Hibberd, M. L., Liu, E. T., Rohwer, F. L., & Ruan, Y. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0040003 · Cited by 799 · see citing works
Kankainen, M., Paulin, L., Tynkkynen, S., von Ossowski, I., Reunanen, J., Partanen, P., Satokari, R., Vesterlund, S., Hendrickx, A. P. A., Lebeer, S., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908876106 · Cited by 740 · see citing works
Intestinal microbiota in human health and disease: the impact of probiotics
Gerritsen, J., Smidt, H., Rijkers, G. T., & de Vos, W. M. (2011) · Genes & Nutrition · doi:10.1007/s12263-011-0229-7 · Cited by 724 · see citing works
Beneficial metabolic effects of a probiotic via butyrate-induced GLP-1 hormone secretion
Yadav, H., Lee, J.-H., Lloyd, J., Walter, P., & Rane, S. G. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.452516 · Cited by 709 · see citing works
Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa
Bron, P. A., van Baarlen, P., & Kleerebezem, M. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2690 · Cited by 690 · see citing works
McNulty, N. P., Yatsunenko, T., Hsiao, A., Faith, J. J., Muegge, B. D., Goodman, A. L., Henrissat, B., Oozeer, R., Cools-Portier, S., Gobert, G., et al. (2011) · Science Translational Medicine · doi:10.1126/scitranslmed.3002701 · Cited by 544 · see citing works
An update on the use and investigation of probiotics in health and disease
Sanders, M. E., Guarner, F., Guerrant, R., Holt, P. R., Quigley, E. M., Sartor, R. B., Sherman, P. M., & Mayer, E. A. (2013) · Gut · doi:10.1136/gutjnl-2012-302504 · Cited by 503 · see citing works
Metatranscriptomic Approach to Analyze the Functional Human Gut Microbiota
Gosalbes, M. J., Durbán, A., Pignatelli, M., Abellan, J. J., Jiménez‐Hernández, N., Pérez‐Cobas, A. E., Latorre, A., & Moyá, A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017447 · Cited by 379 · see citing works
Regulation of intestinal homeostasis and immunity with probiotic lactobacilli
van Baarlen, P., Wells, J. M., & Kleerebezem, M. (2013) · Trends in Immunology · doi:10.1016/j.it.2013.01.005 · Cited by 369 · see citing works
Tackling soil diversity with the assembly of large, complex metagenomes
Howe, A. C., Jansson, J. K., Malfatti, S., Tringe, S. G., Tiedje, J. M., & Brown, C. T. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1402564111 · Cited by 322 · see citing works
Efficient and robust RNA-seq process for cultured bacteria and complex community transcriptomes
Giannoukos, G., Ciulla, D., Huang, K. H., Haas, B. J., Izard, J., Levin, J. Z., Livny, J., Earl, A. M., Gevers, D., Ward, D. V., et al. (2012) · Genome biology · doi:10.1186/gb-2012-13-3-r23 · Cited by 263 · see citing works
von Schillde, M., Hörmannsperger, G., Weiher, M., Alpert, C.-A., Hahne, H., Bäuerl, C., Huynegem, K. V., Steidler, L., Hrnčíř, T., Pérez‐Martínez, G., et al. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.02.006 · Cited by 235 · see citing works
A Reference-Free Algorithm for Computational Normalization of Shotgun Sequencing DataPreprint
Brown, C. T., Howe, A., Zhang, Q., Pyrkosz, A. B., & Brom, T. H. (2012) · arXiv (Cornell University) · doi:10.48550/arxiv.1203.4802 · Cited by 233 · see citing works
Isolation of DNA from bacterial samples of the human gastrointestinal tract
Zoetendal, E. G., Heilig, H. G. H. J., Klaassens, E. S., Booijink, C. C., Kleerebezem, M., Smidt, H., & de Vos, W. M. (2006) · Nature Protocols · doi:10.1038/nprot.2006.142 · Cited by 224 · see citing works
Dedkova, E. N., & Blatter, L. A. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00260 · Cited by 220 · see citing works
Microbial community dynamics in a seasonally anoxic fjord: Saanich Inlet, British Columbia
Zaikova, E., Walsh, D. A., Stilwell, C. P., Mohn, W. W., Tortell, P. D., & Hallam, S. (2009) · Environmental Microbiology · doi:10.1111/j.1462-2920.2009.02058.x · Cited by 211 · see citing works
The Human Microbiome: From Symbiosis to Pathogenesis
Eloe‐Fadrosh, E. A., & Rasko, D. A. (2013) · Annual Review of Medicine · doi:10.1146/annurev-med-010312-133513 · Cited by 210 · see citing works
Self-citationCrystal structure of the Escherichia coli Rob transcription factor in complex with DNA.
Ellenberger, T. E., Kwon, H. J., Bennik, M. H. J., & Demple, B. (2000) · Nature Structural Biology · doi:10.1038/75213 · Cited by 200 · see citing works
Expression patterns reveal niche diversification in a marine microbial assemblage
Gifford, S., Sharma, S., Booth, M. G., & Moran, M. A. (2012) · The ISME Journal · doi:10.1038/ismej.2012.96 · Cited by 200 · see citing works
Lahti, L., Salonen, A., Kekkonen, R. A., Salojärvi, J., Jalanka, J., Palva, A., Orešič, M., & de Vos, W. M. (2013) · PeerJ · doi:10.7717/peerj.32 · Cited by 196 · see citing works
Segawa, S., Fujiya, M., Konishi, H., Ueno, N., Kobayashi, N., Shigyo, T., & Kohgo, Y. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023278 · Cited by 186 · see citing works
Douillard, F. ⁄. O. P., Ribbera, A., rvinen, H. M. J. ⁄., Kant, R., ⁄, T. E. P., Randazzo, C. L., Paulin, L. G., Laine, P., Caggia, C., von Ossowski, I., et al. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.03467-12 · Cited by 126 · see citing works
Isolation of RNA from bacterial samples of the human gastrointestinal tract
Zoetendal, E. G., Booijink, C. C., Klaassens, E. S., Heilig, H. G. H. J., Kleerebezem, M., Smidt, H., & de Vos, W. M. (2006) · Nature Protocols · doi:10.1038/nprot.2006.143 · Cited by 105 · see citing works
Eloe‐Fadrosh, E. A., McArthur, M. A., Seekatz, A. M., Drábek, E. F., Rasko, D. A., Sztein, M. B., & Fraser, C. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062026 · Cited by 104 · see citing works
Self-citationCommunity Health Care: Therapeutic Opportunities in the Human Microbiome
Sonnenburg, J. L., & Fischbach, M. A. (2011) · Science Translational Medicine · doi:10.1126/scitranslmed.3001626 · Cited by 102 · see citing works
Neville, B. A., Sheridan, P. O., Harris, H. M. B., Coughlan, S., Flint, H. J., Duncan, S. H., Jeffery, I. B., Claesson, M. J., Ross, R. P., Scott, K. P., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068919 · Cited by 62 · see citing works
Hibberd, P. L., Kleimola, L., Fiorino, A., Botelho, C. A., Haverkamp, M. R., Andreyeva, I., Poutsiaka, D. D., Fraser, C. M., Solano-Aguilar, G. I., & Snydman, D. R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0113456 · Cited by 52 · see citing works
Self-citationFISH analysis of Lactobacillus biofilms in the gastrointestinal tract of different hosts
Lebeer, S., Verhoeven, T. L. A., Claes, I. J. J., Hertogh, G., Vermeire, S., Buyse, J., Immerseel, F. V., Vanderleyden, J., & Keersmaecker, S. C. J. D. (2010) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2010.02994.x · Cited by 49 · see citing works
Circleator: flexible circular visualization of genome-associated data with BioPerl and SVG
Crabtree, J., Agrawal, S., Mahurkar, A., Myers, G. S. A., Rasko, D. A., & White, O. R. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu505 · Cited by 36 · see citing works
Self-citation
Flagged first, then by citations
1 of the 55 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Influence of diet on the gut microbiome and implications for human health
Singh, R. K., Chang, H.-W., Yan, D., Lee, K. M., Ucmak, D., Wong, K., Abrouk, M., Farahnik, B., Nakamura, M., Zhu, T. H., et al. (2017) · Journal of Translational Medicine · doi:10.1186/s12967-017-1175-y · Cited by 2,599 · see citing works
Rivière, A., Selak, M., Lantin, D., Leroy, F., & Vuyst, L. D. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00979 · Cited by 1,746 · see citing works
Zmora, N., Zilberman-Schapira, G., Suez, J., Mor, U., Dori-Bachash, M., Bashiardes, S., Kotler, E., Zur, M., Regev-Lehavi, D., Brik, R. B.-Z., et al. (2018) · Cell · doi:10.1016/j.cell.2018.08.041 · Cited by 1,695 · see citing works
The central nervous system and the gut microbiome
Sharon, G., Sampson, T. R., Geschwind, D. H., & Mazmanian, S. K. (2016) · Cell · doi:10.1016/j.cell.2016.10.027 · Cited by 1,513 · see citing works
The pros, cons, and many unknowns of probiotics
Suez, J., Zmora, N., Segal, E., & Elinav, E. (2019) · Nature Medicine · doi:10.1038/s41591-019-0439-x · Cited by 1,398 · see citing works
The gut microbiome as a modulator of healthy ageing
Ghosh, T. S., Shanahan, F., & O’Toole, P. W. (2022) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-022-00605-x · Cited by 817 · see citing works
The role of the gut microbiome and its metabolites in metabolic diseases
Wu, J., Wang, K., Wang, X., Pang, Y., & Jiang, C. (2020) · Protein & Cell · doi:10.1007/s13238-020-00814-7 · Cited by 584 · see citing works
Gut microbiota, obesity and diabetes
Patterson, E., Ryan, P. M., Cryan, J. F., Dinan, T. G., Ross, R. P., Fitzgerald, G. F., & Stanton, C. (2016) · Postgraduate Medical Journal · doi:10.1136/postgradmedj-2015-133285 · Cited by 552 · see citing works
Gut microbiota: A player in aging and a target for anti-aging intervention
Vaiserman, A. M., Koliada, A. K., & Marotta, F. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2017.01.001 · Cited by 465 · see citing works
Grosicki, G. J., Fielding, R. A., & Lustgarten, M. S. (2018) · Calcified Tissue International · doi:10.1007/s00223-017-0345-5 · Cited by 388 · see citing works
Thirty Years of Lactobacillus rhamnosus GG
Capurso, L. (2019) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0000000000001170 · Cited by 385 · see citing works
Nagpal, R., Wang, S., Ahmadi, S., Hayes, J., Gagliano, J., Subashchandrabose, S., Kitzman, D. W., Becton, T., Read, R., & Yadav, H. (2018) · Scientific Reports · doi:10.1038/s41598-018-30114-4 · Cited by 355 · see citing works
Qi, X., Zhang, Y., Zhang, Y., Luo, F., Song, K., Wang, G., & Ling, F. (2023) · Microbiome · doi:10.1186/s40168-023-01574-2 · Cited by 302 · see citing works
McBurney, M. I., Davis, C. D., Fraser, C. M., Schneeman, B. O., Huttenhower, C., Verbeke, K., Walter, J., & Latulippe, M. E. (2019) · Journal of Nutrition · doi:10.1093/jn/nxz154 · Cited by 283 · see citing works
Self-citationZhang, J., Sun, Z., Jiang, S., Bai, X., Ma, C., Peng, Q., Chen, K., Chang, H., Fang, T., & Zhang, H. (2019) · mSystems · doi:10.1128/msystems.00017-19 · Cited by 287 · see citing works
Borgeraas, H., Johnson, L. K., Skattebu, J., Hertel, J. K., & Hjelmesæth, J. (2018) · Obesity Reviews · doi:10.1111/obr.12626 · Cited by 278 · see citing works
Microbiota in the Gastrointestinal Tract
Dieterich, W., Schink, M., & Zopf, Y. (2018) · Medical Sciences · doi:10.3390/medsci6040116 · Cited by 269 · see citing works
Zhang, C., Derrien, M., Levenez, F., Brazeilles, R., Ballal, S. A., Kim, J., Degivry, M.-C., Quéré, G., Garault, P., van Hylckama Vlieg, J. E. T., et al. (2016) · The ISME Journal · doi:10.1038/ismej.2016.13 · Cited by 264 · see citing works
Montassier, E., Valdés-Mas, R., Batard, E., Zmora, N., Dori-Bachash, M., Suez, J., & Elinav, E. (2021) · Nature Microbiology · doi:10.1038/s41564-021-00920-0 · Cited by 256 · see citing works
Chahwan, B., Kwan, S., Isik, A., van Hemert, S., Burke, C., & Roberts, L. (2019) · Journal of Affective Disorders · doi:10.1016/j.jad.2019.04.097 · Cited by 256 · see citing works
Xia, Y. L., Lu, M., Chen, G., Cao, J., Gao, F., Wang, M., Liu, Z., Zhang, D., Zhu, H., & Yi, M. (2018) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2018.03.020 · Cited by 243 · see citing works
Bharwani, A., Mian, M. F., Surette, M. G., Bienenstock, J., & Forsythe, P. (2017) · BMC Medicine · doi:10.1186/s12916-016-0771-7 · Cited by 236 · see citing works
Islam, S. U. (2016) · Medicine · doi:10.1097/md.0000000000002658 · Cited by 220 · see citing works
The human gut microbiome in health: Establishment and resilience of microbiota over a lifetime
Greenhalgh, K., Meyer, K. M., Aagaard, K. M., & Wilmes, P. (2016) · Environmental Microbiology · doi:10.1111/1462-2920.13318 · Cited by 218 · see citing works
Gut Dysbiosis and Muscle Aging: Searching for Novel Targets against Sarcopenia
Picca, A., Fanelli, F., Calvani, R., Mulè, G., Pesce, V., Sisto, A., Pantanelli, C., Bernabei, R., Landi, F., & Marzetti, E. (2018) · Mediators of Inflammation · doi:10.1155/2018/7026198 · Cited by 181 · see citing works
Host microbiota can facilitate pathogen infection
Stevens, E. J., Bates, K. A., & King, K. C. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009514 · Cited by 161 · see citing works
Impact of probiotic supplements on microbiome diversity following antibiotic treatment of mice
Grazul, H., Kanda, L. L., & Gondek, D. (2016) · Gut Microbes · doi:10.1080/19490976.2016.1138197 · Cited by 135 · see citing works
Rizzetto, L., Ifrim, D. C., Moretti, S., Tocci, N., Cheng, S., Quintin, J., Renga, G., Oikonomou, V., Filippo, C. D., Weil, T., et al. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.699645 · Cited by 132 · see citing works
Dieterich, W., Schuppan, D., Schink, M., Schwappacher, R., Wirtz, S. J., Agaimy, A., Neurath, M. F., & Zopf, Y. (2018) · Clinical Nutrition · doi:10.1016/j.clnu.2018.03.017 · Cited by 132 · see citing works
Safarchi, A., Al-Qadami, G. H., Tran, C. D., & Conlon, M. A. (2025) · Frontiers in Microbiology · doi:10.3389/fmicb.2025.1559521 · Cited by 133 · see citing works
Burton, K. J., Rosikiewicz, M., Pimentel, G., Bütikofer, U., von Ah, U., Voirol, M.-J., Croxatto, A., Aeby, S., Drai, J., McTernan, P. G., et al. (2017) · British Journal of Nutrition · doi:10.1017/s0007114517000885 · Cited by 121 · see citing works
Yin, Y., Zhang, P., Yue, X., Du, X., Li, W., Yin, Y., Yi, C., & Li, Y. (2018) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2018.06.056 · Cited by 120 · see citing works
Kandasamy, S., Vlasova, A. N., Fischer, D. D., Kumar, A., Chattha, K. S., Rauf, A., Shao, L., Langel, S. N., Rajashekara, G., & Saif, L. J. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1501705 · Cited by 113 · see citing works
The gut microbiota and graft-versus-host disease
Fredricks, D. N. (2019) · Journal of Clinical Investigation · doi:10.1172/jci125797 · Cited by 112 · see citing works
Translating Omics to Food Microbiology
Walsh, A. M., Crispie, F., Claesson, M. J., & Cotter, P. D. (2017) · Annual Review of Food Science and Technology · doi:10.1146/annurev-food-030216-025729 · Cited by 110 · see citing works
Gut Microbiota Interaction with the Central Nervous System throughout Life
Ojeda, J., Ávila, A., & Vidal, P. M. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10061299 · Cited by 107 · see citing works
Liu, H., Hou, C., Wang, G., Jia, H., Yu, H., Zeng, X., Thacker, P. A., Zhang, G., & Qiao, S. (2017) · Nutrients · doi:10.3390/nu9060559 · Cited by 95 · see citing works
Not All Fibers Are Born Equal; Variable Response to Dietary Fiber Subtypes in IBD
Armstrong, H., Mander, I. K., Zhang, Z., Armstrong, D. W. J., & Wine, E. (2021) · Frontiers in Pediatrics · doi:10.3389/fped.2020.620189 · Cited by 92 · see citing works
Wang, J., Tang, L., Zhou, J., Zhou, J., Glenn, T. C., Shen, C., & Wang, J.-S. (2018) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2018.01.005 · Cited by 89 · see citing works
Interventions on Gut Microbiota for Healthy Aging
Zeppa, S. D., Agostini, D., Ferrini, F., Gervasi, M., Barbieri, E., Bartolacci, A., Piccoli, G., Saltarelli, R., Sestili, P., & Stocchi, V. (2022) · Cells · doi:10.3390/cells12010034 · Cited by 91 · see citing works
Mills, S., Lane, J. A., Smith, G. J., Grimaldi, K. A., Ross, R. P., & Stanton, C. (2019) · Nutrients · doi:10.3390/nu11071468 · Cited by 88 · see citing works
The microbiota-gut-brain axis: Focus on the fundamental communication pathways
Bistoletti, M., Bosi, A., Banfi, D., Giaroni, C., & Baj, A. (2020) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2020.08.012 · Cited by 88 · see citing works
Wu, Y., & Zhang, G. (2018) · LWT · doi:10.1016/j.lwt.2018.03.034 · Cited by 83 · see citing works
Probiotics in the next-generation sequencing era
Suez, J., Zmora, N., & Elinav, E. (2019) · Gut Microbes · doi:10.1080/19490976.2019.1586039 · Cited by 82 · see citing works
Barkhidarian, B., Roldos, L., Iskandar, M. M., Saedisomeolia, A., & Kubow, S. J. (2021) · Nutrients · doi:10.3390/nu13093001 · Cited by 77 · see citing works
Matijašić, B. B., Obermajer, T., Lipoglavšek, L., Sernel, T., Locatelli, I., Kos, M., Šmid, A., & Rogelj, I. (2016) · Journal of Dairy Science · doi:10.3168/jds.2015-10743 · Cited by 79 · see citing works
Hudson, L. E., Anderson, S. E., Corbett, A. H., & Lamb, T. J. (2016) · Clinical Microbiology Reviews · doi:10.1128/cmr.00049-16 · Cited by 76 · see citing works
Vuholm, S., Nielsen, D. S., Iversen, K., Suhr, J., Westermann, P., Krych, Ł., Andersen, J. R., & Kristensen, M. (2017) · Journal of Nutrition · doi:10.3945/jn.117.250647 · Cited by 74 · see citing works
McCarville, J. L., Dong, J., Caminero, A., Bermudez-Brito, M., Jury, J., Murray, J. A., Duboux, S., Steinmann, M., Delley, M., Tangyu, M., et al. (2017) · Applied and Environmental Microbiology · doi:10.1128/aem.01323-17 · Cited by 71 · see citing works
Probiotics and microbiota composition
Sanders, M. E. (2016) · BMC Medicine · doi:10.1186/s12916-016-0629-z · Cited by 72 · see citing works
Role of Probiotics, Prebiotics, and Synbiotics in the Elderly: Insights Into Their Applications
Ale, E. C., & Binetti, A. G. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.631254 · Cited by 64 · see citing works
Major Depressive Disorder and gut microbiota – Association not causation. A scoping review
Łoniewski, I., Misera, A., Skonieczna‐Żydecka, K., Kaczmarczyk, M., Kaźmierczak-Siedlecka, K., Misiak, B., Marlicz, W. M., & Samochowiec, J. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110111 · Cited by 63 · see citing works
Scalabrin, D., Harris, C. L., Johnston, W., & Berseth, C. L. (2016) · European Journal of Pediatrics · doi:10.1007/s00431-016-2825-4 · Cited by 61 · see citing works
Odamaki, T., Kato, K., Sugahara, H., Xiao, J., Abe, F., & Benno, Y. (2016) · Beneficial Microbes · doi:10.3920/bm2015.0173 · Cited by 59 · see citing works
Wang, N., Gao, C., Zhang, P., Guan, L., Wang, Y., Qin, Y., & Li, Y. (2019) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2019.03.047 · Cited by 57 · see citing works
Bioactive compounds of foods: Phytochemicals and peptides
Xavier, J. R., Sanjay, B. S., Gupta, D., Mehta, S., & Chauhan, O. P. (2024) · Food and Humanity · doi:10.1016/j.foohum.2024.100354 · Cited by 52 · see citing works
Bifidobacterium adolescentis supplementation attenuates fracture-induced systemic sequelae
Roberts, J. L., Liu, G., Darby, T. M., Fernandes, L. M., Díaz‐Hernández, M. E., Jones, R. M., & Drissi, H. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110831 · Cited by 52 · see citing works
Amat, S., Alexander, T. W., Holman, D. B., Schwinghamer, T. D., & Timsit, E. (2020) · mSystems · doi:10.1128/msystems.00629-19 · Cited by 47 · see citing works
Antibiotic-induced dysbiosis of the rat oral and gut microbiota and resistance to Salmonella
Wu, H., Ma, Y., Peng, X., Qiu, W., Kong, L., Ren, B., Li, M., Cheng, G., Zhou, X., & Cheng, L. (2020) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2020.104730 · Cited by 47 · see citing works
A Survey on Antimicrobial Resistance Genes of Frequently Used Probiotic Bacteria, 1901 to 2022
Tóth, A. G., Judge, M. F., Nagy, S. Á., Papp, M., & Solymosi, N. (2023) · Eurosurveillance · doi:10.2807/1560-7917.es.2023.28.14.2200272 · Cited by 46 · see citing works
Probiotic strains and mechanistic insights for the treatment of type 2 diabetes
Hampe, C. S., & Roth, C. L. (2017) · Endocrine · doi:10.1007/s12020-017-1433-z · Cited by 45 · see citing works
Plé, C., Richoux, R., Jardin, J., Nurdin, M., Briard‐Bion, V., Parayre, S., Ferreira, S., Pot, B., Bouguen, G., Deutsch, S., et al. (2015) · Journal of Functional Foods · doi:10.1016/j.jff.2015.08.015 · Cited by 44 · see citing works
Exploring the Preventive Effect and Mechanism of Senile Sarcopenia Based on “Gut–Muscle Axis”
Liao, X., Wu, M., Hao, Y., & Hong, D. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.590869 · Cited by 44 · see citing works
Liu, T., Song, X., An, Y., Wu, X., Zhang, W., Li, J., Sun, Y., Jin, G., Liu, X., Guo, Z., et al. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/3328505 · Cited by 42 · see citing works
Zhao, J., Liang, R., Song, Q., Song, S., Yue, J., & Wu, C. (2023) · Precision Clinical Medicine · doi:10.1093/pcmedi/pbad010 · Cited by 38 · see citing works
Kaczmarczyk, M., Szulińska, M., Łoniewski, I., Kręgielska-Narożna, M., Skonieczna‐Żydecka, K., Kościółek, T., Bezshapkin, V., & Bogdański, P. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.815798 · Cited by 40 · see citing works
Bifidobacterium longum supplementation improves age‐related delays in fracture repair
Roberts, J. L., Golloshi, M., Harding, D. B., Conduah, M., Liu, G., & Drissi, H. (2023) · Aging Cell · doi:10.1111/acel.13786 · Cited by 37 · see citing works
Metabolic fluorine labeling and hotspot imaging of dynamic gut microbiota in mice
Chen, D., Guo, J., Li, A., Sun, C., Lin, H., Lin, H., Yang, C. J., Wang, W., & Gao, J. (2023) · Science Advances · doi:10.1126/sciadv.abg6808 · Cited by 37 · see citing works
Recent Advances in Anti-Aging Medicine
Son, D., Park, W.-J., & Lee, Y. (2019) · Korean Journal of Family Medicine · doi:10.4082/kjfm.19.0087 · Cited by 37 · see citing works
Laroute, V., Beaufrand, C., Gomes, P., Nouaille, S., Tondereau, V., Daveran‐Mingot, M., Théodorou, V., Eutamène, H., Mercier‐Bonin, M., & Cocaign‐Bousquet, M. (2022) · eLife · doi:10.7554/elife.77100 · Cited by 37 · see citing works
Alvarez, A.-S., Tap, J., Chambaud, I., Cools-Portier, S., Quinquis, L., Bourlioux, P., Marteau, P., Guillemard, E., Schrezenmeir, J., & Derrien, M. (2020) · Scientific Reports · doi:10.1038/s41598-020-72161-w · Cited by 36 · see citing works
Sanders, M. E., & Hill, C. (2025) · Cell Host & Microbe · doi:10.1016/j.chom.2025.04.017 · Cited by 36 · see citing works
Misera, A., Liśkiewicz, P., Łoniewski, I., Skonieczna-Żydecka, K., & Samochowiec, J. (2021) · Pharmaceuticals · doi:10.3390/ph14100952 · Cited by 34 · see citing works
Aktaş, B., Wolfe, T. J. D., Tandee, K., Safdar, N., Darien, B. J., & Steele, J. L. (2015) · PLoS ONE · doi:10.1371/journal.pone.0145784 · Cited by 34 · see citing works
Flach, J., van der Waal, M. B., Kardinaal, A. F. M., Schloesser, J. E. L., Ruijschop, R. M. A. J., & Claassen, E. (2018) · Cogent Food & Agriculture · doi:10.1080/23311932.2018.1452839 · Cited by 34 · see citing works
Microbiota Targeted Interventions of Probiotic Lactobacillus as an Anti-Ageing Approach: A Review
Ishaq, M., Khan, A., Bacha, A. S., Shah, T., Hanif, A., Ahmad, A. A., Ke, W., Li, F., Din, A. U., Ding, Z., et al. (2021) · Antioxidants · doi:10.3390/antiox10121930 · Cited by 34 · see citing works
Nutrient pollution alters the gut microbiome of a territorial reef fish
Degregori, S., Casey, J. M., & Barber, P. H. (2021) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2021.112522 · Cited by 33 · see citing works
Shang, X., Wang, B., Sun, Q., Zhang, Y., Lu, Y., Liu, S., & Li, Y. (2022) · Fish Physiology and Biochemistry · doi:10.1007/s10695-022-01046-8 · Cited by 33 · see citing works
Gut Microbiota Alteration After Long-Term Consumption of Probiotics in the Elderly
Gao, R., Zhang, X., Huang, L., Shen, R., & Qin, H. (2018) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-018-9403-1 · Cited by 32 · see citing works
Origination, change, and modulation of geriatric disease-related gut microbiota during life
Rajoka, M. S. R., Zhao, H., Li, N., Lu, Y. P., Lian, Z., Shao, D., Jin, M., Li, Q., Zhao, L., & Shi, J. (2018) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-018-9264-2 · Cited by 32 · see citing works
Sanders, M. E., Goh, Y. J., & Klaenhammer, T. R. (2019) · ASM Press eBooks · doi:10.1128/9781555819972.ch32 · Cited by 32 · see citing works
Message in a Bottle: Dialog between Intestine and Skin Modulated by Probiotics
Friedrich, A. D., Paz, M. L., Leoni, J., & Maglio, D. H. G. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18061067 · Cited by 31 · see citing works
Zhang, Y., Brady, A., Jones, C. E., Song, Y., Darton, T. C., Jones, C., Blohmke, C. J., Pollard, A. J., Magder, L. S., Fasano, A., et al. (2018) · mBio · doi:10.1128/mbio.00686-18 · Cited by 31 · see citing works
Self-citationPagnini, C., Paolo, M. C. D., Urgesi, R., PALLOTTA, L., Fanello, G., Graziani, M. G., & Fave, G. D. (2023) · Microorganisms · doi:10.3390/microorganisms11061381 · Cited by 30 · see citing works
Ni, Y., Wong, V. H. Y., Tai, W. C. S., Li, J., Wong, W. Y., Lee, M. M. L., Fong, F. L. Y., El-Nezami, H., & Panagiotou, G. (2017) · Journal of Applied Microbiology · doi:10.1111/jam.13386 · Cited by 29 · see citing works
Bautista‐Gallego, J., Ferrocino, I., Botta, C., Ercolini, D., Cocolin, L., & Rantsiou, K. (2019) · Food Research International · doi:10.1016/j.foodres.2019.02.004 · Cited by 29 · see citing works
Biodiversity of Intestinal Lactic Acid Bacteria in the Healthy Population
Mikelsaar, M., Sepp, E., Štšepetova, J., Songisepp, E., & Mändar, R. (2016) · Advances in experimental medicine and biology · doi:10.1007/5584_2016_3 · Cited by 29 · see citing works
Gorbach, S. L., Doron, S., & Magro, F. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-804024-9.00007-0 · Cited by 28 · see citing works
Abildgaard, A. M., Kern, T., Pedersen, O. B., Hansen, T. F., Wegener, G., & Lund, S. A. (2018) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2018.10.011 · Cited by 29 · see citing works
Cross-Kingdom Similarities in Microbiome Ecology and Biocontrol of Pathogens
Berg, G., Krause, R. G. E., & Mendes, R. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.01311 · Cited by 27 · see citing works
Lavrinienko, A., Scholier, T., Bates, S. T., Miller, A. N., & Watts, P. C. (2021) · Animal Microbiome · doi:10.1186/s42523-021-00134-z · Cited by 27 · see citing works
Li, L., Fang, Z., Lee, Y. K., Zhao, J., Zhang, H., Peng, H., Zhang, Y., Lu, W., & Chen, W. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.862934 · Cited by 27 · see citing works
He, Q., Hou, Q., Wang, Y., Shen, L., Sun, Z., Zhang, H., Liong, M., & Kwok, L. (2019) · Journal of Functional Foods · doi:10.1016/j.jff.2019.103682 · Cited by 26 · see citing works
Metagenomic and metatranscriptomic profiling of Lactobacillus casei Zhang in the human gut
Wang, J., Zhang, J., Liu, W., Zhang, H., & Sun, Z. (2021) · npj Biofilms and Microbiomes · doi:10.1038/s41522-021-00227-2 · Cited by 25 · see citing works
Abildgaard, A. M., Kern, T., Pedersen, O. B., Hansen, T. F., Lund, S. A., & Wegener, G. (2020) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2020.09.001 · Cited by 24 · see citing works
Tan, T., Ba, Z., Sanders, M. E., D'Amico, F. J., Roberts, R., Smith, K. H., & Merenstein, D. J. (2016) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000001272 · Cited by 24 · see citing works
Du, S., Chen, W., Yao, Z., Huang, X., Chen, C., Guo, H., & Zhang, D. (2021) · Animal Microbiome · doi:10.1186/s42523-021-00152-x · Cited by 22 · see citing works
Tong, J., Satyanarayanan, S. K., & Su, H. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.08.027 · Cited by 24 · see citing works
Postbiotics: A Promising Approach to Combat Age-Related Diseases
Hamdi, A., Lloyd, C., Eri, R. D., & Van, T. T. H. (2025) · Life · doi:10.3390/life15081190 · Cited by 24 · see citing works
Sadeghi, J., Chaganti, S. R., & Heath, D. D. (2023) · Molecular Ecology · doi:10.1111/mec.17039 · Cited by 20 · see citing works
- Authors
- Eloe-Fadrosh, E. A., Brady, A., Crabtree, J., Drabek, E. F., Ma, B., Mahurkar, A., Ravel, J., Haverkamp, M., Fiorino, A.-M., Botelho, C., Andreyeva, I., Hibberd, P. L., & Fraser, C. M.
- Affiliations
- Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, USA
- University of Maryland, Baltimore (US)
- Massachusetts General Hospital (US)
- Corresponding author
- Fraser, Claire M.
- ORCID
- Venue
- mBio
- Publisher
- American Society for Microbiology
- Published
- 2015-05
- Volume
- 6
- Issue
- 2
- ISSN
- 2150-7511 (ISSN-L)
- 2161-2129
- PMC
- PMC4453556
- OpenAlex
- W2156573030
- Cited by
- 160
- References
- 55
- Citations by year
- 2026: 3 · 2025: 11 · 2024: 8 · 2023: 11 · 2022: 14 · 2021: 21 · 2020: 11 · 2019: 19 · 2018: 20 · 2017: 19 · 2016: 19 · 2015: 4
- FWCI
- 27.59
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- mBio (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Science Foundation (0959894)
- National Institutes of Health
- National Center for Complementary and Alternative Medicine
- National Center for Complementary and Integrative Health (K24AT003683, U01AT002952, U01AT002133, U01AT002388)
- 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
- Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
- Keywords
- probiotics, Lactobacillus rhamnosus GG, gut microbiota, older adults, Bifidobacterium, Roseburia, Eubacterium, flagellar motility, chemotaxis, adhesion, host-microbe interactions, anti-inflammatory pathways, interindividual variability, 16S rRNA gene profiling
- MeSH terms
- Gastrointestinal Microbiome, Aged, Aged, 80 and over, DNA, Bacterial, DNA, Ribosomal, Female, Humans, Male, Molecular Sequence Data, Phylogeny, RNA, Ribosomal, 16S, Cluster Analysis, Sequence Analysis, DNA, Probiotics, Gene Expression Profiling, Gastrointestinal Tract, Lacticaseibacillus rhamnosus, Microbial Interactions
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