Dysbiosis in the inflamed intestine: Chance favors the prepared microbe
Open accessAbstract
The bacterial microbiota of the human large bowel is a complex ecosystem consisting of several hundred, mostly anaerobic, species. To maintain colonization of the gut lumen and maximize growth in the presence of nutritional competitors, highly diverse metabolic pathways have evolved, with each microbe utilizing a different "winning strategy" for nutrient acquisition and utilization. Conditions and diseases leading to intestinal inflammation are accompanied by a severe disruption the microbiota composition characterized by an expansion of facultative anaerobic Enterobacteriaceae. Here, we review evidence that the local inflammatory response creates a unique nutritional environment that is conducive to a bloom of bacterial species whose genomes encode the capability of utilizing inflammation-derived nutrients.
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Dysbiosis of the Firmicutes:Bacteroidetes ratio heralds a shift in microbiota from obligate anaerobes to nitrate-reducing, facultative anaerobes of the Proteobacteria and Firmicutes phyla.
“Characteristically, dysbiosis of this ratio heralds a shift in microbiota from obligate anaerobes to nitrate-reducing, facultative anaerobes of the Proteobacteria and Firmicutes phyla[333–335].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [334]
In inflammatory bowel disease, massive blooms of pathogenic, nitrate-reducing Salmonella and Escherichia coli are seen in response to inflammation.
“This shift is particularly notable in the context of inflammatory bowel disease, where massive blooms of pathogenic, nitrate-reducing Salmonella and Escherichia coli are seen in response to inflammation[333,334,338,339].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [334]
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Cites
KEGG: Kyoto Encyclopedia of Genes and Genomes
Kanehisa, M. (2000) · Nucleic Acids Research · doi:10.1093/nar/28.1.27 · Cited by 37,077 · see citing works
KEGG: Kyoto Encyclopedia of Genes and Genomes
Ogata, H., Goto, S., Sato, K., Fujibuchi, W., Bono, H., & Kanehisa, M. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.1.29 · Cited by 31,232 · see citing works
Diversity of the Human Intestinal Microbial Flora
Eckburg, P. B., Bik, E. M., Bernstein, C. N., Purdom, E., Dethlefsen, L., Sargent, M., Gill, S. R., Nelson, K. E., & Relman, D. A. (2005) · Science · doi:10.1126/science.1110591 · Cited by 7,913 · see citing works
KEGG for integration and interpretation of large-scale molecular data sets
Kanehisa, M., Goto, S., Sato, Y., Furumichi, M., & Tanabe, M. (2012) · Nucleic Acids Research · doi:10.1093/nar/gkr988 · Cited by 4,848 · see citing works
Frank, D. N., St. Amand, A. L., Feldman, R. A., Boedeker, E. C., Harpaz, N., & Pace, N. R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706625104 · Cited by 4,611 · see citing works
Peroxynitrite: biochemistry, pathophysiology and development of therapeutics
Szabó, C., Ischiropoulos, H., & Radi, R. (2007) · Nature Reviews Drug Discovery · doi:10.1038/nrd2222 · Cited by 2,134 · see citing works
Lupp, C., Robertson, M. L., Wickham, M. E., Sekirov, I., Champion, O. L., Gaynor, E. C., & Finlay, B. B. (2007) · Cell Host & Microbe · doi:10.1016/j.chom.2007.06.010 · Cited by 1,310 · see citing works
Gut inflammation provides a respiratory electron acceptor for Salmonella
Winter, S., Thiennimitr, P., Winter, M. G., Butler, B. P., Huseby, D. L., Crawford, R. W., Russell, J. M., Bevins, C. L., Adams, L. G., Tsolis, R. M., et al. (2010) · Nature · doi:10.1038/nature09415 · Cited by 1,271 · see citing works
Stecher, B., Robbiani, R., Walker, A. W., Westendorf, A. M., Barthel, M., Kremer, M., Chaffron, S., Macpherson, A. J., Buer, J., Parkhill, J., et al. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050244 · Cited by 1,048 · see citing works
Host-Derived Nitrate Boosts Growth of <i>E. coli</i> in the Inflamed Gut
Winter, S. E., Winter, M. G., Xavier, M. N., Thiennimitr, P., Poon, V., Keestra, A. M., Laughlin, R. C., Gomez, G., Wu, J., Lawhon, S. D., et al. (2013) · Science · doi:10.1126/science.1232467 · Cited by 1,019 · see citing works
Commensal bacteria at the interface of host metabolism and the immune system
Brestoff, J. R., & Artis, D. (2013) · Nature Immunology · doi:10.1038/ni.2640 · Cited by 945 · see citing works
Garrett, W. S., Gallini, C. A., Yatsunenko, T., Michaud, M., DuBois, A., Delaney, M. L., Punit, S., Karlsson, M., Bry, L., Glickman, J. N., et al. (2010) · Cell Host & Microbe · doi:10.1016/j.chom.2010.08.004 · Cited by 788 · see citing works
Alterations of the dominant faecal bacterial groups in patients with Crohn's disease of the colon
Seksik, P., Rigottier‐Gois, L., Gramet, G., BRIEND‐SUTREN, M., Pochart, P., Marteau, P. R., Jian, R., & Dore, J. M. (2003) · Gut · doi:10.1136/gut.52.2.237 · Cited by 746 · see citing works
Gastrointestinal microbiome signatures of pediatric patients with irritable bowel syndrome
Saulnier, D. M., Riehle, K., Mistretta, T., Diaz, M., Mandal, D., Raza, S., Weidler, E. M., Qin, X., Coarfa, C., Milosavljevic, A., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.06.072 · Cited by 672 · see citing works
Innate immune recognition of the microbiota promotes host-microbial symbiosis
Chu, H., & Mazmanian, S. K. (2013) · Nature Immunology · doi:10.1038/ni.2635 · Cited by 630 · see citing works
Baumgart, M., Dogan, B., Rishniw, M., Weitzman, G., Bosworth, B. P., Yantiss, R. K., Orsi, R. H., Wiedmann, M., McDonough, P. L., Kim, S. G., et al. (2007) · The ISME Journal · doi:10.1038/ismej.2007.52 · Cited by 630 · see citing works
Gophna, U., Sommerfeld, K., Gophna, S., Doolittle, W., & van Zanten, S. V. (2006) · Journal of Clinical Microbiology · doi:10.1128/jcm.01004-06 · Cited by 541 · see citing works
Bactericidal activity of peroxynitrite
Zhu, L., Gunn, C., & Beckman, J. S. (1992) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(92)90434-x · Cited by 438 · see citing works
Enteric Salmonellosis Disrupts the Microbial Ecology of the Murine Gastrointestinal Tract
Barman, M., Unold, D., Shifley, K., Amir, E., Hung, K.-C., Bos, N. A., & Salzman, N. H. (2007) · Infection and Immunity · doi:10.1128/iai.01432-07 · Cited by 428 · see citing works
Carroll, I. M., Ringel‐Kulka, T., Siddle, J. P., & Ringel, Y. (2012) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2012.01891.x · Cited by 425 · see citing works
Wlodarska, M., Willing, B., Keeney, K. M., Menendez, A., Bergstrom, K. S., Gill, N., Russell, S. L., Vallance, B. A., & Finlay, B. B. (2011) · Infection and Immunity · doi:10.1128/iai.01104-10 · Cited by 382 · see citing works
Krogius-Kurikka, L., Lyra, A., Malinen, E., Aarnikunnas, J., Tuimala, J., Paulin, L. G., Mäkivuokko, H., Kajander, K., & Palva, A. (2009) · BMC Gastroenterology · doi:10.1186/1471-230x-9-95 · Cited by 307 · see citing works
Mättö, J., Maunuksela, L., Kajander, K., Palva, A., Korpela, R., Kassinen, A., & Saarela, M. (2005) · FEMS Immunology & Medical Microbiology · doi:10.1016/j.femsim.2004.08.009 · Cited by 301 · see citing works
Genetic and redox determinants of nitric oxide cytotoxicity in a Salmonella typhimurium model.
Groote, M. A. D., Granger, D., Xu, Y., Campbell, G., Prince, R. W., & Fang, F. C. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.14.6399 · Cited by 250 · see citing works
Lopez, C. A., Winter, S., Rivera-Chávez, F., Byndloss, M. X., Poon, V., Nuccio, S., Tsolis, R. M., & Bäumler, A. J. (2012) · mBio · doi:10.1128/mbio.00143-12 · Cited by 242 · see citing works
Spees, A. M., Wangdi, T., Lopez, C. A., Kingsbury, D. D., Byndloss, M. X., Winter, S., Tsolis, R. M., & Bäumler, A. J. (2013) · mBio · doi:10.1128/mbio.00430-13 · Cited by 237 · see citing works
Raetz, M. M., Hwang, S., Wilhelm, C. L., Kirkland, D., Benson, A., Sturge, C. R., Mirpuri, J., Vaishnava, S., Hou, B., DeFranco, A. L., et al. (2012) · Nature Immunology · doi:10.1038/ni.2508 · Cited by 217 · see citing works
Intraluminal Containment of Commensal Outgrowth in the Gut during Infection-Induced Dysbiosis
Molloy, M. J., Grainger, J. R., Bouladoux, N. J., Hand, T. W., Koo, L. Y., Naik, S., Quiñones, M., Dzutsev, A., Gao, J., Trinchieri, G., et al. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.08.003 · Cited by 156 · see citing works
Haag, L.-M., Fischer, A., Otto, B., Plickert, R., Kühl, A. A., Göbel, U. B., Bereswill, S., & Heimesaat, M. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035988 · Cited by 133 · see citing works
Normann, E., Fahlén, A., Engstrand, L. G., & Lilja, H. E. (2012) · Acta Paediatrica · doi:10.1111/apa.12059 · Cited by 128 · see citing works
Kerckhoffs, A. P. M., Amor, K. B., Samsom, M., van der Rest, M. E., de Vogel, J., Knol, J., & Akkermans, L. M. A. (2010) · Journal of Medical Microbiology · doi:10.1099/jmm.0.022848-0 · Cited by 124 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The Oral Microbiota: Dynamic Communities and Host Interactions
Lamont, R. J., Koo, H., & Hajishengallis, G. (2018) · Nature Reviews Microbiology · doi:10.1038/s41579-018-0089-x · Cited by 2,217 · see citing works
Garrett, W. S. (2015) · Science · doi:10.1126/science.aaa4972 · Cited by 1,404 · see citing works
Gut Microbiome: Profound Implications for Diet and Disease
Hills, R. D., Pontefract, B., Mishcon, H. R., Black, C. A., Sutton, S. C., & Theberge, C. R. (2019) · Nutrients · doi:10.3390/nu11071613 · Cited by 1,107 · see citing works
Gut Microbiota Dysbiosis in Postweaning Piglets: Understanding the Keys to Health
Gresse, R., Chaucheyras‐Durand, F., Fleury, M., de Wiele, T. V., Forano, É., & Blanquet‐Diot, S. (2017) · Trends in Microbiology · doi:10.1016/j.tim.2017.05.004 · Cited by 903 · see citing works
Lewis, J. D., Chen, E. Z., Baldassano, R. N., Otley, A. R., Griffiths, A. M., Lee, D., Bittinger, K., Bailey, A., Friedman, E. S., Hoffmann, C., et al. (2015) · Cell Host & Microbe · doi:10.1016/j.chom.2015.09.008 · Cited by 823 · see citing works
The respiratory tract microbiome and lung inflammation: a two-way street.
Huffnagle, G. B., Dickson, R. P., & Lukacs, N. W. (2017) · Mucosal Immunology · doi:10.1038/mi.2016.108 · Cited by 535 · see citing works
Novel mechanisms and functions of complement
Hajishengallis, G., Reis, E. S., Mastellos, D. C., Ricklin, D., & Lambris, J. D. (2017) · Nature Immunology · doi:10.1038/ni.3858 · Cited by 484 · see citing works
Microplastics and the gut microbiome: How chronically exposed species may suffer from gut dysbiosis
Fackelmann, G., & Sommer, S. (2019) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2019.04.030 · Cited by 385 · see citing works
Parker, A., Romano, S., Ansorge, R., Aboelnour, A., Le Gall, G., Savva, G. M., Pontifex, M. G., Telatin, A., Baker, D., Jones, E., et al. (2022) · Microbiome · doi:10.1186/s40168-022-01243-w · Cited by 368 · see citing works
Current concepts in the pathogenesis of periodontitis: from symbiosis to dysbiosis
Abdulkareem, A. A., Al-Taweel, F. B. H., Al-Sharqi, A. J. B., Gul, S. S., Sha, A. M., & Chapple, I. (2023) · Journal of Oral Microbiology · doi:10.1080/20002297.2023.2197779 · Cited by 402 · see citing works
Dong, H., Chen, Y., Wang, J., Zhang, Y., Zhang, P., Li, X., Zou, J., & Zhou, A. (2020) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2020.123961 · Cited by 346 · see citing works
Hajishengallis, G., & Lamont, R. J. (2021) · Periodontology 2000 · doi:10.1111/prd.12371 · Cited by 302 · see citing works
Plastics and the microbiome: impacts and solutions
Lear, G., Kingsbury, J. M., Franchini, S., Gambarini, V. M. D. O., Maday, S. D. M., Wallbank, J. A., Weaver, L., & Pantos, O. (2021) · Environmental Microbiome · doi:10.1186/s40793-020-00371-w · Cited by 288 · see citing works
Borgo, F., Riva, A., Benetti, A., Casiraghi, M. C., Bertelli, S., Garbossa, S., Anselmetti, S., Scarone, S., Pontiroli, A. E., Morace, G., et al. (2017) · PLOS ONE · doi:10.1371/journal.pone.0179739 · Cited by 267 · see citing works
Linking the Microbiota, Chronic Disease, and the Immune System
Hand, T. W., Vujkovic-Cvijin, I., Ridaura, V. K., & Belkaid, Y. (2016) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2016.08.003 · Cited by 247 · see citing works
“One view on the etiology of these diseases is that barrier and immune dysfunction leads to an outgrowth of those organisms capable of withstanding the intestinal inflammatory response [43].”
BackgroundIrritable bowel syndrome, the microbiota and the gut-brain axis
Raskov, H., Burcharth, J., Pommergaard, H.-C., & Rosenberg, J. (2016) · Gut Microbes · doi:10.1080/19490976.2016.1218585 · Cited by 243 · see citing works
Dysbiotic Events in Gut Microbiota: Impact on Human Health
Schippa, S., & Conte, M. (2014) · Nutrients · doi:10.3390/nu6125786 · Cited by 247 · see citing works
Metabolic crosstalk between host and pathogen: sensing, adapting and competing
Olive, A. J., & Sassetti, C. M. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.12 · Cited by 228 · see citing works
Metabolomic and microbiome profiling reveals personalized risk factors for coronary artery disease
Talmor‐Barkan, Y., Bar, N., Shaul, A. A., Shahaf, N., Godneva, A., Bussi, Y., Lotan‐Pompan, M., Weinberger, A., Shechter, A., Chezar‐Azerrad, C., et al. (2022) · Nature Medicine · doi:10.1038/s41591-022-01686-6 · Cited by 218 · see citing works
Wang, Z., Wang, Q., Wang, X., Zhu, L., Chen, J., Zhang, B., Chen, Y., & Yuan, Z. (2019) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.14289 · Cited by 195 · see citing works
Koch, C. D., Gladwin, M. T., Freeman, B. A., Lundberg, J. O., Weitzberg, E., & Morris, A. (2017) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.12.015 · Cited by 186 · see citing works
Pathogens, microbiome and the host: emergence of the ecological Koch's postulates
Vonaesch, P., Anderson, M. C., & Sansonetti, P. J. (2018) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuy003 · Cited by 170 · see citing works
Constante, M., Fragoso, G., Calvé, A., Samba-Mondonga, M., & Santos, M. M. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01809 · Cited by 161 · see citing works
“Enterobacteriaceae and Escherichia coli levels increased (Figure 2).”
BackgroundInfluentialChiodini, R. J., Dowd, S. E., Chamberlin, W., Galandiuk, S., Davis, B. R., & Glassing, A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0134382 · Cited by 160 · see citing works
The plant NADPH oxidase RBOHD is required for microbiota homeostasis in leaves
Pfeilmeier, S., Petti, G. C., Bortfeld‐Miller, M., Daniel, B. B. J., Field, C. M., Sunagawa, S., & Vorholt, J. A. (2021) · Nature Microbiology · doi:10.1038/s41564-021-00929-5 · Cited by 155 · see citing works
Recipient factors in faecal microbiota transplantation: one stool does not fit all
Danne, C., Rolhion, N., & Sokol, H. (2021) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-021-00441-5 · Cited by 154 · see citing works
Giardia Alters Commensal Microbial Diversity throughout the Murine Gut
Barash, N. R., Maloney, J. G., Singer, S. M., & Dawson, S. C. (2017) · Infection and Immunity · doi:10.1128/iai.00948-16 · Cited by 150 · see citing works
The Pyromaniac Inside You: Salmonella Metabolism in the Host Gut
Rivera-Chávez, F., & Bäumler, A. J. (2015) · Annual Review of Microbiology · doi:10.1146/annurev-micro-091014-104108 · Cited by 143 · see citing works
Linking Gut Microbiota to Colorectal Cancer
Raskov, H., Burcharth, J., & Pommergaard, H. (2017) · Journal of Cancer · doi:10.7150/jca.20497 · Cited by 151 · see citing works
Intestinal dysbiosis in children with short bowel syndrome is associated with impaired outcome
Engstrand Lilja, H., Wefer, H., Nyström, N., Finkel, Y., & Engstrand, L. (2015) · Microbiome · doi:10.1186/s40168-015-0084-7 · Cited by 145 · see citing works
Grazing practices affect the soil microbial community composition in a Tibetan alpine meadow
Yang, F., Niu, K., Collins, C. G., Yan, X., Ji, Y., Ling, N., Zhou, X., Du, G., Guo, H. J., & Hu, S. (2018) · Land Degradation and Development · doi:10.1002/ldr.3189 · Cited by 126 · see citing works
Zhu, W., Miyata, N., Winter, M. G., Arenales, A., Hughes, E. R., Spiga, L., Kim, J., Sifuentes-Dominguez, L., Starokadomskyy, P., Gopal, P., et al. (2019) · The Journal of Experimental Medicine · doi:10.1084/jem.20181939 · Cited by 124 · see citing works
“This is consistent with the idea that increased availability of respiratory electron acceptors in the gut lumen facilitates a restructuring of the microbial community structure during inflammation (Winter and B¨aumler, 2014; Byndloss et al., 2018).”
Microbiome or Infections: Amyloid-Containing Biofilms as a Trigger for Complex Human Diseases
Miller, A. L., Bessho, S., Grando, K. C. M., & Tükel, Ç. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.638867 · Cited by 131 · see citing works
“Facultative anaerobic pathogens and pathobiont strains thrive in an inflammatory environment due to their ability to utilize inflammation-derived molecules such as nitrites and oxides as electron acceptors (199).”
BackgroundThe Microbiota of the Extremely Preterm Infant
Underwood, M. A., & Sohn, K. (2017) · Clinics in Perinatology · doi:10.1016/j.clp.2017.01.005 · Cited by 123 · see citing works
Microbial imbalance and intestinal pathologies: connections and contributions
Yang, Y., & Jobin, C. (2014) · Disease Models & Mechanisms · doi:10.1242/dmm.016428 · Cited by 112 · see citing works
Inflammation: A Double-Edged Sword in the Response to Pseudomonas aeruginosa Infection
Lin, C. K., & Kazmierczak, B. I. (2017) · Journal of Innate Immunity · doi:10.1159/000455857 · Cited by 113 · see citing works
A tale of two sites: how inflammation can reshape the microbiomes of the gut and lungs
Scales, B. S., Dickson, R. P., & Huffnagle, G. B. (2016) · Journal of Leukocyte Biology · doi:10.1189/jlb.3mr0316-106r · Cited by 109 · see citing works
Learning from bacterial competition in the host to develop antimicrobials
Raffatellu, M. (2018) · Nature Medicine · doi:10.1038/s41591-018-0145-0 · Cited by 110 · see citing works
Targeting Bacterial Biofilms by the Green Tea Polyphenol EGCG
Hengge, R. (2019) · Molecules · doi:10.3390/molecules24132403 · Cited by 104 · see citing works
Li, K., Chen, Z., Huang, Y. H., Zhang, R., Luan, X.-Q., Lei, T., & Chen, L. (2019) · Respiratory Research · doi:10.1186/s12931-019-1246-0 · Cited by 106 · see citing works
Xenosiderophore Utilization Promotes Bacteroides thetaiotaomicron Resilience during Colitis
Zhu, W., Winter, M. G., Spiga, L., Hughes, E. R., Chanin, R. B., Mulgaonkar, A., Pennington, J., Maas, M., Behrendt, C. L., Kim, J., et al. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.01.010 · Cited by 100 · see citing works
Zhang, P., Lu, G., Sun, Y., Yan, Z., Dang, T., & Liu, J. (2021) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2021.127773 · Cited by 103 · see citing works
The impact of intestinal inflammation on the nutritional environment of the gut microbiota
Faber, F., & Bäumler, A. J. (2014) · Immunology Letters · doi:10.1016/j.imlet.2014.04.014 · Cited by 92 · see citing works
Vázquez-Torres, A., & Bäumler, A. J. (2016) · Current Opinion in Microbiology · doi:10.1016/j.mib.2015.09.002 · Cited by 92 · see citing works
“Furthermore, among the phylogenetic groupings that have been described within gut-associated microbial communities, the frequency at which a predicted nitrate reductase activity is present within genomes is highest for the Enterobacteriaceae [22].”
BackgroundInfluentialProtective and pro-inflammatory roles of intestinal bacteria
Webb, C. R., Koboziev, I., Furr, K. L., & Grisham, M. B. (2016) · Pathophysiology · doi:10.1016/j.pathophys.2016.02.002 · Cited by 94 · see citing works
Dunn, K. A., Moore-Connors, J., MacIntyre, B., Stadnyk, A. W., Thomas, N. A., Noble, A. J., Mahdi, G., Rashid, M., Otley, A. R., Bielawski, J. P., et al. (2016) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000956 · Cited by 93 · see citing works
Folate Acts in E. coli to Accelerate C. elegans Aging Independently of Bacterial Biosynthesis
Virk, B., Jia, J., Maynard, C., Raimundo, A., Lefebvre, J., Richards, S. A., Chetina, N., Liang, Y., Helliwell, N., Cipinska, M., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.01.051 · Cited by 92 · see citing works
Impact of systemic factors in shaping the periodontal microbiome
Teles, F., Wang, Y., Hajishengallis, G., Hastürk, H., & Marchesan, J. T. (2020) · Periodontology 2000 · doi:10.1111/prd.12356 · Cited by 89 · see citing works
Production and Function of Immunoglobulin A
Hand, T. W., & Reboldi, A. (2021) · Annual Review of Immunology · doi:10.1146/annurev-immunol-102119-074236 · Cited by 88 · see citing works
Shen, J., Wang, S., He, X., Han, S., Wang, Q., Wu, Z., Zhuge, A., Li, S., Chen, H., Lv, L., et al. (2023) · Food & Function · doi:10.1039/d3fo04051h · Cited by 86 · see citing works
GAS6 is a key homeostatic immunological regulator of host–commensal interactions in the oral mucosa
Nassar, M., Tabib, Y., Capucha, T., Mizraji, G., Nir, T., Pevsner‐Fischer, M., Zilberman-Schapira, G., Heyman, O., Nussbaum, G., Bercovier, H., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1614926114 · Cited by 85 · see citing works
Fecal Microbiota Changes in Patients With Postpartum Depressive Disorder
Zhou, Y., Chen, C., Yu, H., & Yang, Z. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.567268 · Cited by 81 · see citing works
“Overgrowth of Enterbacteriaceae could result in gut inflammation and increased permeability of the gut wall, which in turn favors bacterial translocation, promoting systemic inflammation (Winter and Bäumler, 2014).”
BackgroundMooney, J. P., Lokken, K. L., Byndloss, M. X., George, M. D., Velazquez, E. M., Faber, F., Butler, B. P., Walker, G. T., Ali, M. M., Potts, R. A., et al. (2015) · Scientific Reports · doi:10.1038/srep14603 · Cited by 79 · see citing works
Vongbhavit, K., & Underwood, M. A. (2016) · Clinical Therapeutics · doi:10.1016/j.clinthera.2016.01.006 · Cited by 79 · see citing works
Xie, M., Lin, L., Xu, P., Zhou, W., Zhao, C., Ding, D., & Suo, A. (2021) · Ecological Indicators · doi:10.1016/j.ecolind.2021.108370 · Cited by 78 · see citing works
From food to cell: nutrient exploitation strategies of enteropathogens
Staib, L., & Fuchs, T. M. (2014) · Microbiology · doi:10.1099/mic.0.078105-0 · Cited by 76 · see citing works
Gut Microbiome: Profound Implications for Diet and Disease
Hills, R. D., Pontefract, B., Mishcon, H. R., Black, C. A., Sutton, S. C., & Theberge, C. R. (2022) · Kompass Nutrition & Dietetics · doi:10.1159/000523712 · Cited by 79 · see citing works
“In IBD, respiratory electron acceptors generated as a byproduct of the inflammatory host response become environmental stressors that support bacterial growth [20].”
BackgroundRhizosphere pseudomonads as probiotics improving plant health
Kim, Y. C., & Anderson, A. J. (2018) · Molecular Plant Pathology · doi:10.1111/mpp.12693 · Cited by 72 · see citing works
“Indeed, disease symptoms in the gut, such as irritable bowel disease, or on the skin, are cor- related with a lack of certain microbial colonizers and effective levels of others (Raskov et al., 2016; Winter and Baumler, 2014).”
BackgroundSpiga, L., Fansler, R. T., Perera, Y. R., Shealy, N. G., Munneke, M. J., David, H. E., Torres, T. P., Lemoff, A. S., Ran, X., Richardson, K. L., et al. (2023) · Cell Host & Microbe · doi:10.1016/j.chom.2023.08.018 · Cited by 71 · see citing works
Dr. NO and Mr. Toxic – the versatile role of nitric oxide
Porrini, C., Ramarao, N., & Tran, S. (2019) · Biological Chemistry · doi:10.1515/hsz-2019-0368 · Cited by 70 · see citing works
“Thereafter, by analyzing more than 2000 genomes of the gut-associated microbiota, it has been shown that Enterobacteriaceae present the highest prevalence of nitrate reductase activity and are therefore the most potent to use nitrate for their growth (Winter and Baumler, 2014).”
BackgroundKunath, B. J., Hickl, O., Queirós, P., Martin‐Gallausiaux, C., Lebrun, L., Halder, R., Laczny, C. C., Schmidt, T., Hayward, M. R., Becher, D., et al. (2022) · Microbiome · doi:10.1186/s40168-022-01435-4 · Cited by 69 · see citing works
Kovtun, A. S., Averina, O. V., Angelova, I. Y., Yunes, R. А., Zorkina, Y., Morozova, A. Y., Pavlichenko, A. V., Syunyakov, T., Karpenko, O., Kostyuk, G. P., et al. (2022) · Biomedicines · doi:10.3390/biomedicines10092162 · Cited by 67 · see citing works
Fundora, J. B., Guha, P., Shores, D. R., Pammi, M., & Maheshwari, A. (2019) · Pediatric Research · doi:10.1038/s41390-019-0482-9 · Cited by 60 · see citing works
van Dorst, J. M., Tam, R. Y., & Ooi, C. Y. (2022) · Nutrients · doi:10.3390/nu14030480 · Cited by 60 · see citing works
Pathobiology of Salmonella, Intestinal Microbiota, and the Host Innate Immune Response
Santos, R. L. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00252 · Cited by 59 · see citing works
Collateral Damage: Microbiota-Derived Metabolites and Immune Function in the Antibiotic Era
Lopez, C. A., Kingsbury, D. D., Velazquez, E. M., & Bäumler, A. J. (2014) · Cell Host & Microbe · doi:10.1016/j.chom.2014.07.009 · Cited by 59 · see citing works
The Multifaceted Role of Commensal Microbiota in Homeostasis and Gastrointestinal Diseases
Silva, M. J. B., Carneiro, M. B. H., Pultz, B. D. A., Silva, D. P., Lopes, M. E., & dos Santos, L. M. (2015) · Journal of Immunology Research · doi:10.1155/2015/321241 · Cited by 58 · see citing works
Tam, R. Y., van Dorst, J. M., McKay, I. R., Coffey, M. J., & Ooi, C. Y. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11030649 · Cited by 58 · see citing works
Ajibola, O., Rowan-Nash, A. D., Ogedengbe, C. O., Mshelia, M. B., Cabral, D. J., Eze, A. A., Obaro, S., & Belenky, P. A. (2019) · Scientific Reports · doi:10.1038/s41598-018-36709-1 · Cited by 51 · see citing works
The Microbiota and the Immune Response: What Is the Chicken and What Is the Egg?
Fritsch, J., & Abreu, M. T. (2019) · Gastrointestinal Endoscopy Clinics of North America · doi:10.1016/j.giec.2019.02.005 · Cited by 52 · see citing works
Gu, L., Deng, H., Ren, Z., Zhao, Y., Yu, S., Guo, Y., Dai, J., Chen, X., Li, K., Li, R., et al. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.02491 · Cited by 49 · see citing works
Nutritional Modulation of the Microbiome and Immune Response
Burr, A. B. P., Bhattacharjee, A., & Hand, T. W. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.2000419 · Cited by 49 · see citing works
Probiotic Streptococcus salivarius K12 Alleviates Radiation-Induced Oral Mucositis in Mice
Wang, Y., Li, J., Zhang, H., Zheng, X. M., Wang, J., Jia, X., Peng, X., Xie, Q., Zou, J., Zheng, L., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.684824 · Cited by 47 · see citing works
Crosstalk between microbiota, pathogens and the innate immune responses
Günther, C., Josenhans, C., & Wehkamp, J. (2016) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2016.03.003 · Cited by 48 · see citing works
Duan, J., Meng, X., Liu, S., Zhou, P., Zeng, C., Fu, C., Dou, Q., Wu, A., & Li, C. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00190 · Cited by 46 · see citing works
“Additionally, the abundances of two taxa (Saccharomycetes and Clostridia) were significantly lower in CDpD in comparison with control.”
BackgroundInfluentialKuang, J., Huang, Y., Hu, J., Yu, J., Zhou, Q., & Liu, D. (2020) · Journal of Functional Foods · doi:10.1016/j.jff.2020.104212 · Cited by 45 · see citing works
Temperate phages promote colicin‐dependent fitness of S almonella enterica serovar T yphimurium
Nedialkova, L., Sidstedt, M., Koeppel, M. B., Spriewald, S., Ring, D., Gerlach, R. G., Bossi, L., & Stecher, B. (2015) · Environmental Microbiology · doi:10.1111/1462-2920.13077 · Cited by 43 · see citing works
Neto, J. C. G., Kittana, H., Mantz, S., Muñoz, R. R. S., Schmaltz, R. J., Bindels, L. B., Clarke, J., Hostetter, J. M., Benson, A. K., Walter, J., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-18014-5 · Cited by 42 · see citing works
Dual role of heme iron in cancer; promotor of carcinogenesis and an inducer of tumour suppression
Gamage, S. M. K., Lee, K. T., Dissabandara, L., Lam, A. K.-Y., & Gopalan, V. (2021) · Experimental and Molecular Pathology · doi:10.1016/j.yexmp.2021.104642 · Cited by 42 · see citing works
Wang, T., Shi, C., Wang, S., Zhang, Y., Wang, S., Ismael, M., Zhang, J., Wang, X., & Lü, X. (2022) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.1c07316 · Cited by 40 · see citing works
The Airway Microbiome-IL-17 Axis: a Critical Regulator of Chronic Inflammatory Disease
Mannion, J. M., McLoughlin, R. M., & Lalor, S. J. (2022) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-022-08928-y · Cited by 42 · see citing works
Murine Models of Salmonella Infection
Walker, G. T., Gerner, R. R., Nuccio, S., & Raffatellu, M. (2023) · Current Protocols · doi:10.1002/cpz1.824 · Cited by 39 · see citing works
“Microbiota-activated PPAR-γ signaling inhibits dysbiotic Enterobacteriaceae expansion.”
BackgroundInfluentialShelton, C. D., & Byndloss, M. X. (2020) · Infection and Immunity · doi:10.1128/iai.00939-19 · Cited by 39 · see citing works
The Lung Microbiome: A Central Mediator of Host Inflammation and Metabolism in Lung Cancer Patients?
Weinberg, F. D., Dickson, R. P., Nagrath, D., & Ramnath, N. (2020) · Cancers · doi:10.3390/cancers13010013 · Cited by 38 · see citing works
Microbiota and Drug Response in Inflammatory Bowel Disease
Franzin, M., Stefančič, K., Lucafò, M., Decorti, G., & Stocco, G. (2021) · Pathogens · doi:10.3390/pathogens10020211 · Cited by 39 · see citing works
“As a consequence, it has been noticed that in IBD there is a reduction in obligately anaerobic bacteria (class Clostridia belonging to the Firmicutes phylum and class Bacteroidia belonging to the Bacteroidetes phylum) and a parallel increase in facultatively anaerobic bacteria (family Enterobacteriaceae belonging to t…”
BackgroundSpero, M. A., & Newman, D. K. (2018) · mBio · doi:10.1128/mbio.01400-18 · Cited by 38 · see citing works
Oliveira, E. C. S. D., Quaglio, A. E. V., Magro, D. O., Stasi, L. C. D., & Sassaki, L. Y. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24087176 · Cited by 37 · see citing works
“On the other hand, in IBD patients, the by-products of the host’s inflammatory response become environmental stressors, favoring bacterial growth [1,54].”
BackgroundZakrzewski, M., Simms, L. A., Brown, A., Appleyard, M. N., Irwin, J. R., Waddell, N., & Radford‐Smith, G. L. (2018) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjy188 · Cited by 36 · see citing works
Yanguas‐Casás, N., Torres‐Fuentes, C., Crespo‐Castrillo, A., Díaz-Pacheco, S., Healy, K., Stanton, C., Chowen, J. A., García‐Segura, L. M., Arévalo, M., Cryan, J. F., et al. (2021) · Neurobiology of Disease · doi:10.1016/j.nbd.2021.105495 · Cited by 36 · see citing works
Intestinal dysbacteriosis leads to kidney stone disease
Zhao, E., Zhang, W., Geng, B., You, B., Wang, W., & Li, X. (2020) · Molecular Medicine Reports · doi:10.3892/mmr.2020.11819 · Cited by 33 · see citing works
Impact of Gut Microbiota on the Association between Diet and Depressive Symptoms in Breast Cancer
Maitiniyazi, G., Cao, X., Chen, Y., Zhang, R., Liu, Y., Li, Z., Gu, D., Li, T., & Xia, S. (2022) · Nutrients · doi:10.3390/nu14061186 · Cited by 33 · see citing works
Burcher, K. M., Burcher, J. T., Inscore, L., Bloomer, C. H., Furdui, C. M., & Porosnicu, M. (2022) · Cancers · doi:10.3390/cancers14174116 · Cited by 32 · see citing works
Carolak, E., Czajkowska, J., Stypułkowska, A., Waszczuk, W., Dutkiewicz, A., & Grzymajło, K. (2025) · Gut Microbes · doi:10.1080/19490976.2025.2519696 · Cited by 31 · see citing works
A Bacterial Inflammation Sensor Regulates c-di-GMP Signaling, Adhesion, and Biofilm Formation
Perkins, A., Tudorica, D. A., Teixeira, R. D., Schirmer, T., Zumwalt, L., Ogba, O. M., Cassidy, C. K., Stansfeld, P. J., & Guillemin, K. J. (2021) · mBio · doi:10.1128/mbio.00173-21 · Cited by 29 · see citing works
Chiodini, R. J., Dowd, S. E., Galandiuk, S., Davis, B. R., & Glassing, A. (2016) · Microbiology · doi:10.1099/mic.0.000336 · Cited by 30 · see citing works
Impact of gut microbiota on plasma oxylipins profile under healthy and obesogenic conditions
Ávila‐Román, J., Arreaza‐Gil, V., Cortés-Espinar, A. J., Soliz‐Rueda, J. R., Mulero, M., Muguerza, B., Arola‐Arnal, A., Arola, L., & Torres‐Fuentes, C. (2021) · Clinical Nutrition · doi:10.1016/j.clnu.2021.02.035 · Cited by 30 · see citing works
Tashiro, H., & Shore, S. A. (2021) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2020-0288tr · Cited by 32 · see citing works
Fujimoto, M., Goto, R., Haneda, T., Okada, N., & Miki, T. (2018) · Infection and Immunity · doi:10.1128/iai.00280-18 · Cited by 28 · see citing works
Glucosylation Drives the Innate Inflammatory Response to Clostridium difficile Toxin A
Cowardin, C. A., Jackman, B. M., Noor, Z., Burgess, S. L., Feig, A. L., & Petri, W. A. (2016) · Infection and Immunity · doi:10.1128/iai.00327-16 · Cited by 28 · see citing works
Muhummed, A. M., Lanker, K. C., Yersin, S., Zinsstag, J., & Vonaesch, P. (2025) · Microbiome · doi:10.1186/s40168-025-02231-6 · Cited by 27 · see citing works
- Authors
- Winter, S. E., & Bäumler, A. J.
- Affiliations
- University of California, Davis (US)
- Corresponding author
- Bäumler, Andreas J
- Venue
- Gut Microbes
- Publisher
- Informa UK Limited
- Published
- 2014-01
- Volume
- 5
- Issue
- 1
- Pages
- 71-73
- ISSN
- 1949-0976 (ISSN-L)
- 1949-0984
- PMC
- PMC4049941
- OpenAlex
- W1968113723
- Cited by
- 194
- References
- 31
- Citations by year
- 2026: 15 · 2025: 14 · 2024: 9 · 2023: 17 · 2022: 30 · 2021: 23 · 2020: 15 · 2019: 16 · 2018: 10 · 2017: 14 · 2016: 15 · 2015: 10 · 2014: 6
- FWCI
- 6.15
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Gut Microbes (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (AI103248, R21AI103248, R21AI107393, AI096528, AI107393, R01AI096528)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Health Sciences › Medicine › Infectious Diseases › Clostridium difficile and Clostridium perfringens research
- Keywords
- gut dysbiosis, intestinal inflammation, gut microbiota, Enterobacteriaceae, facultative anaerobes, nutrient acquisition, anaerobic bacteria, host-microbe interactions
- MeSH terms
- Animals, Colitis, Escherichia coli, Intestine, Large, Nitrates
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