Interbacterial mechanisms of colonization resistance and the strategies pathogens use to overcome them

Sekirov, 2010, Gut microbiota in health and disease, Physiol. Rev., 90, 859, 10.1152/physrev.00045.2009 Hasegawa, 2010, Transitions in oral and intestinal microflora composition and innate immune receptor-dependent stimulation during mouse development, Infect. Immun., 78, 639, 10.1128/IAI.01043-09 Palmer, 2007, Development of the human infant intestinal microbiota, PLoS Biol., 5, e177, 10.1371/journal.pbio.0050177 Kim, 2017, Neonatal acquisition of Clostridia species protects against colonization by bacterial pathogens, Science, 356, 315, 10.1126/science.aag2029 Yatsunenko, 2012, Human gut microbiome viewed across age and geography, Nature, 486, 222, 10.1038/nature11053 Human Microbiome Project, C., 2012, Structure, function and diversity of the healthy human microbiome, Nature, 486, 207, 10.1038/nature11234 Turnbaugh, 2009, A core gut microbiome in obese and lean twins, Nature, 457, 480, 10.1038/nature07540 Qin, 2010, A human gut microbial gene catalogue established by metagenomic sequencing, Nature, 464, 59, 10.1038/nature08821 Rivera-Chavez, 2015, The pyromaniac inside you: Salmonella metabolism in the host gut, Annu. Rev. Microbiol, 69, 31, 10.1146/annurev-micro-091014-104108 Abt, 2016, Clostridium difficile colitis: pathogenesis and host defence, Nat. Rev. Microbiol, 14, 609, 10.1038/nrmicro.2016.108 Taur, 2012, Intestinal domination and the risk of bacteremia in patients undergoing allogeneic hematopoietic stem cell transplantation, Clin. Infect. Dis., 55, 905, 10.1093/cid/cis580 Ubeda, 2010, Vancomycin-resistant Enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans, J. Clin. Invest., 120, 4332, 10.1172/JCI43918 Centers for Disease Control and Prevention. Antibiotic Resistance Threats in the United States. 2013. https://www.cdc.gov/drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf Bohnhoff, 1964, Resistance of the mouse's intestinal tract to experimental Salmonella infection. I. Factors which interfere with the initiation of infection by oral inoculation, J. Exp. Med., 120, 805, 10.1084/jem.120.5.805 Bohnhoff, 1954, Effect of streptomycin on susceptibility of intestinal tract to experimental Salmonella infection, Proc. Soc. Exp. Biol. Med., 86, 132, 10.3181/00379727-86-21030 Rabiu, 2002, Carbohydrates: a limit on bacterial diversity within the colon, Biol. Rev. Camb. Philos. Soc., 77, 443, 10.1017/S1464793102005961 Friesen, 2004, Experimental evidence for sympatric ecological diversification due to frequency-dependent competition in Escherichia coli, Evolution, 58, 245 Crombach, 2009, Evolution of resource cycling in ecosystems and individuals, BMC Evol. Biol., 9, 122, 10.1186/1471-2148-9-122 Freter, 1983, Mechanisms that control bacterial populations in continuous-flow culture models of mouse large intestinal flora, Infect. Immun., 39, 676, 10.1128/iai.39.2.676-685.1983 Pereira, 2017, Microbial nutrient niches in the gut, Environ. Microbiol., 19, 1366, 10.1111/1462-2920.13659 Stecher, 2010, Like will to like: abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria, PLoS Pathog., 6, e1000711, 10.1371/journal.ppat.1000711 Kamada, 2012, Regulated virulence controls the ability of a pathogen to compete with the gut microbiota, Science, 336, 1325, 10.1126/science.1222195 Fabich, 2008, Comparison of carbon nutrition for pathogenic and commensal Escherichia coli strains in the mouse intestine, Infect. Immun., 76, 1143, 10.1128/IAI.01386-07 Chang, 2004, Carbon nutrition of Escherichia coli in the mouse intestine, Proc. Natl. Acad. Sci. USA, 101, 7427, 10.1073/pnas.0307888101 Maltby, 2013, Nutritional basis for colonization resistance by human commensal Escherichia coli strains HS and Nissle 1917 against E. coli O157:H7 in the mouse intestine, PLoS ONE, 8, e53957, 10.1371/journal.pone.0053957 Leatham, 2009, Precolonized human commensal Escherichia coli strains serve as a barrier to E. coli O157:H7 growth in the streptomycin-treated mouse intestine, Infect. Immun., 77, 2876, 10.1128/IAI.00059-09 Sonnenburg, 2010, Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations, Cell, 141, 1241, 10.1016/j.cell.2010.05.005 Sonnenburg, 2016, Diet-induced extinctions in the gut microbiota compound over generations, Nature, 529, 212, 10.1038/nature16504 Smits, 2017, Seasonal cycling in the gut microbiome of the Hadza hunter-gatherers of Tanzania, Science, 357, 802, 10.1126/science.aan4834 Deriu, 2013, Probiotic bacteria reduce salmonella typhimurium intestinal colonization by competing for iron, Cell Host Microbe, 14, 26, 10.1016/j.chom.2013.06.007 Gielda, 2012, Zinc competition among the intestinal microbiota, MBio, 3, e00112, 10.1128/mBio.00171-12 Sassone-Corsi, 2016, Siderophore-based immunization strategy to inhibit growth of enteric pathogens, Proc. Natl. Acad. Sci. USA, 113, 13462, 10.1073/pnas.1606290113 Martinez-Augustin, 2008, Intestinal bile acid physiology and pathophysiology, World J. Gastroenterol., 14, 5630, 10.3748/wjg.14.5630 Russell, 2003, The enzymes, regulation, and genetics of bile acid synthesis, Annu. Rev. Biochem, 72, 137, 10.1146/annurev.biochem.72.121801.161712 Urdaneta, 2017, Interactions between bacteria and bile salts in the gastrointestinal and hepatobiliary tracts, Front. Med. (Lausanne), 4, 163, 10.3389/fmed.2017.00163 Kang, 2008, Clostridium scindens baiCD and baiH genes encode stereo-specific 7alpha/7beta-hydroxy-3-oxo-delta4-cholenoic acid oxidoreductases, Biochim. Biophys. Acta, 1781, 16, 10.1016/j.bbalip.2007.10.008 Wilson, 1983, Efficiency of various bile salt preparations for stimulation of Clostridium difficile spore germination, J. Clin. Microbiol., 18, 1017, 10.1128/jcm.18.4.1017-1019.1983 Buffie, 2015, Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile, Nature, 517, 205, 10.1038/nature13828 Koenigsknecht, 2015, Dynamics and establishment of Clostridium difficile infection in the murine gastrointestinal tract, Infect. Immun., 83, 934, 10.1128/IAI.02768-14 Theriot, C. M., Bowman, A. A. & Young, V. B. Antibiotic-induced alterations of the gut microbiota alter secondary bile acid production and allow for Clostridium difficile spore germination and outgrowth in the large intestine. mSphere.1, 1–16 (2016). https://doi.org/10.1128/mSphere.00045-15 Lewis, B. B. et al. Pathogenicity locus, core genome, and accessory gene contributions to Clostridium difficile virulence. MBio.8, 1–15 (2017). https://doi.org/10.1128/mBio.00885-17 Lewis, 2016, Bile acid sensitivity and in vivo virulence of clinical Clostridium difficile isolates, Anaerobe, 41, 32, 10.1016/j.anaerobe.2016.05.010 Flint, 2015, Links between diet, gut microbiota composition and gut metabolism, Proc. Nutr. Soc., 74, 13, 10.1017/S0029665114001463 Morrison, 2016, Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism, Gut Microbes, 7, 189, 10.1080/19490976.2015.1134082 Topping, 2001, Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides, Physiol. Rev., 81, 1031, 10.1152/physrev.2001.81.3.1031 Macfarlane, 2003, Regulation of short-chain fatty acid production, Proc. Nutr. Soc., 62, 67, 10.1079/PNS2002207 Ruppin, 1980, Absorption of short-chain fatty acids by the colon, Gastroenterology, 78, 1500, 10.1016/S0016-5085(19)30508-6 Farmer, 2014, Caecal pH is a biomarker of excessive colonic fermentation, World J. Gastroenterol., 20, 5000, 10.3748/wjg.v20.i17.5000 Cherrington, 1991, Short-chain organic acids at ph 5.0 kill Escherichia coli and Salmonella spp. without causing membrane perturbation, J. Appl. Bacteriol., 70, 161, 10.1111/j.1365-2672.1991.tb04442.x Roe, 2002, Inhibition of Escherichia coli growth by acetic acid: a problem with methionine biosynthesis and homocysteine toxicity, Microbiology, 148, 2215, 10.1099/00221287-148-7-2215 Roe, 1998, Perturbation of anion balance during inhibition of growth of Escherichia coli by weak acids, J. Bacteriol., 180, 767, 10.1128/JB.180.4.767-772.1998 Olsan, 2017, Colonization resistance: the deconvolution of a complex trait, J. Biol. Chem., 292, 8577, 10.1074/jbc.R116.752295 Rivera-Chavez, 2016, Depletion of Butyrate-producing Clostridia from the gut microbiota drives an aerobic luminal expansion of Salmonella, Cell Host Microbe, 19, 443, 10.1016/j.chom.2016.03.004 Byndloss, 2017, Microbiota-activated PPAR-gamma signaling inhibits dysbiotic Enterobacteriaceae expansion, Science, 357, 570, 10.1126/science.aam9949 Alex, 2013, Short-chain fatty acids stimulate angiopoietin-like 4 synthesis in human colon adenocarcinoma cells by activating peroxisome proliferator-activated receptor gamma, Mol. Cell. Biol., 33, 1303, 10.1128/MCB.00858-12 Kelly, 2015, Crosstalk between microbiota-derived short-chain fatty acids and intestinal epithelial HIF augments tissue barrier function, Cell Host Microbe, 17, 662, 10.1016/j.chom.2015.03.005 Lawhon, 2002, Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA, Mol. Microbiol., 46, 1451, 10.1046/j.1365-2958.2002.03268.x Hung, 2013, The intestinal fatty acid propionate inhibits Salmonella invasion through the post-translational control of HilD, Mol. Microbiol, 87, 1045, 10.1111/mmi.12149 Durant, 2000, Short-chain volatile fatty acids modulate the expression of the hilA and invF genes of Salmonella typhimurium, J. Food Prot., 63, 573, 10.4315/0362-028X-63.5.573 Gantois, 2006, Butyrate specifically down-regulates salmonella pathogenicity island 1 gene expression, Appl. Environ. Microbiol., 72, 946, 10.1128/AEM.72.1.946-949.2006 Fischbach, 2006, Assembly-line enzymology for polyketide and nonribosomal peptide antibiotics: logic, machinery, and mechanisms, Chem. Rev., 106, 3468, 10.1021/cr0503097 Park, 2011, Discovery of parallel pathways of kanamycin biosynthesis allows antibiotic manipulation, Nat. Chem. Biol., 7, 843, 10.1038/nchembio.671 Janata, 2015, Lincosamide synthetase—a unique condensation system combining elements of nonribosomal peptide synthetase and mycothiol metabolism, PLoS ONE, 10, e0118850, 10.1371/journal.pone.0118850 Arnison, 2013, Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature, Nat. Prod. Rep., 30, 108, 10.1039/C2NP20085F Asaduzzaman, 2009, Lantibiotics: diverse activities and unique modes of action, J. Biosci. Bioeng., 107, 475, 10.1016/j.jbiosc.2009.01.003 Breukink, 1999, Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic, Science, 286, 2361, 10.1126/science.286.5448.2361 Corr, 2007, Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118, Proc. Natl. Acad. Sci. USA, 104, 7617, 10.1073/pnas.0700440104 Rea, 2010, Thuricin CD, a posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile, Proc. Natl. Acad. Sci. USA, 107, 9352, 10.1073/pnas.0913554107 Brunati, 2018, Expanding the potential of NAI-107 for treating serious ESKAPE pathogens: synergistic combinations against Gram-negatives and bactericidal activity against non-dividing cells, J. Antimicrob. Chemother., 73, 414, 10.1093/jac/dkx395 Vukomanovic, 2017, Nano-engineering the antimicrobial spectrum of lantibiotics: activity of Nisin against Gram negative bacteria, Sci. Rep., 7, 10.1038/s41598-017-04670-0 Zhou, 2016, Potentiating the Activity of Nisin against Escherichia coli, Front. Cell Dev. Biol., 4, 7, 10.3389/fcell.2016.00007 Donia, 2014, A systematic analysis of biosynthetic gene clusters in the human microbiome reveals a common family of antibiotics, Cell, 158, 1402, 10.1016/j.cell.2014.08.032 Tomita, 1997, Cloning and genetic and sequence analyses of the bacteriocin 21 determinant encoded on the Enterococcus faecalis pheromone-responsive conjugative plasmid pPD1, J. Bacteriol., 179, 7843, 10.1128/jb.179.24.7843-7855.1997 Martinez-Bueno, 1990, A transferable plasmid associated with AS-48 production in Enterococcus faecalis, J. Bacteriol., 172, 2817, 10.1128/jb.172.5.2817-2818.1990 Tomita, 1996, Cloning and genetic organization of the bacteriocin 31 determinant encoded on the Enterococcus faecalis pheromone-responsive conjugative plasmid pYI17, J. Bacteriol., 178, 3585, 10.1128/jb.178.12.3585-3593.1996 Clewell, 1993, Bacterial sex pheromone-induced plasmid transfer, Cell, 73, 9, 10.1016/0092-8674(93)90153-H Gilmore, 2015, Pheromone killing of multidrug-resistant Enterococcus faecalis V583 by native commensal strains, Proc. Natl. Acad. Sci. USA, 112, 7273, 10.1073/pnas.1500553112 Kommineni, 2015, Bacteriocin production augments niche competition by enterococci in the mammalian gastrointestinal tract, Nature, 526, 719, 10.1038/nature15524 Vimont, 2017, Bacteriocin-producing Enterococcus faecium LCW 44: a high potential probiotic candidate from raw camel milk, Front. Microbiol., 8, 865, 10.3389/fmicb.2017.00865 Frank, 2010, The human nasal microbiota and Staphylococcus aureus carriage, PLoS ONE, 5, e10598, 10.1371/journal.pone.0010598 Bessesen, 2015, MRSA colonization and the nasal microbiome in adults at high risk of colonization and infection, J. Infect., 71, 649, 10.1016/j.jinf.2015.08.008 Zipperer, 2016, Human commensals producing a novel antibiotic impair pathogen colonization, Nature, 535, 511, 10.1038/nature18634 Duquesne, 2007, Microcins, gene-encoded antibacterial peptides from enterobacteria, Nat. Prod. Rep., 24, 708, 10.1039/b516237h Patzer, 2003, The colicin G, H and X determinants encode microcins M and H47, which might utilize the catecholate siderophore receptors FepA, Cir, Fiu and IroN, Microbiology, 149, 2557, 10.1099/mic.0.26396-0 Sassone-Corsi, 2016, Microcins mediate competition among Enterobacteriaceae in the inflamed gut, Nature, 540, 280, 10.1038/nature20557 Roelofs, K. G. et al. Bacteroidales secreted antimicrobial proteins target surface molecules necessary for gut colonization and mediate competition in vivo. MBio.7, 1–10 (2016). https://doi.org/10.1128/mBio.01055-16 Chatzidaki-Livanis, 2014, An antimicrobial protein of the gut symbiont Bacteroides fragilis with a MACPF domain of host immune proteins, Mol. Microbiol., 94, 1361, 10.1111/mmi.12839 Chatzidaki-Livanis, M. et al. Gut symbiont Bacteroides fragilis secretes a eukaryotic-like ubiquitin protein that mediates intraspecies antagonism. MBio.8, 1–12 (2017). https://doi.org/10.1128/mBio.01902-17 Cascales, 2007, Colicin biology, Microbiol. Mol. Biol. Rev., 71, 158, 10.1128/MMBR.00036-06 Kirkup, 2004, Antibiotic-mediated antagonism leads to a bacterial game of rock-paper-scissors in vivo, Nature, 428, 412, 10.1038/nature02429 Silverman, 2012, Structure and regulation of the type VI secretion system, Annu. Rev. Microbiol., 66, 453, 10.1146/annurev-micro-121809-151619 Chen, 2015, Composition, function, and regulation of T6SS in Pseudomonas aeruginosa, Microbiol Res., 172, 19, 10.1016/j.micres.2015.01.004 Russell, 2011, Type VI secretion delivers bacteriolytic effectors to target cells, Nature, 475, 343, 10.1038/nature10244 Whitney, 2015, An interbacterial NAD(P)(+) glycohydrolase toxin requires elongation factor Tu for delivery to target cells, Cell, 163, 607, 10.1016/j.cell.2015.09.027 Russell, 2014, Type VI secretion system effectors: poisons with a purpose, Nat. Rev. Microbiol, 12, 137, 10.1038/nrmicro3185 Russell, 2014, A type VI secretion-related pathway in Bacteroidetes mediates interbacterial antagonism, Cell Host Microbe, 16, 227, 10.1016/j.chom.2014.07.007 Coyne, 2014, Evidence of extensive DNA transfer between bacteroidales species within the human gut, MBio, 5, e01305, 10.1128/mBio.01305-14 Coyne, 2016, Type VI secretion systems of human gut Bacteroidales segregate into three genetic architectures, two of which are contained on mobile genetic elements, BMC Genom., 17, 10.1186/s12864-016-2377-z Verster, 2017, The landscape of type VI secretion across human gut microbiomes reveals its role in community composition, Cell Host Microbe, 22, 411, 10.1016/j.chom.2017.08.010 Chatzidaki-Livanis, 2016, Bacteroides fragilis type VI secretion systems use novel effector and immunity proteins to antagonize human gut Bacteroidales species, Proc. Natl. Acad. Sci. USA, 113, 3627, 10.1073/pnas.1522510113 Wexler, 2016, Human symbionts inject and neutralize antibacterial toxins to persist in the gut, Proc. Natl. Acad. Sci. USA, 113, 3639, 10.1073/pnas.1525637113 Hecht, 2016, Strain competition restricts colonization of an enteric pathogen and prevents colitis, EMBO Rep., 17, 1281, 10.15252/embr.201642282 Whitney, J. C. et al. A broadly distributed toxin family mediates contact-dependent antagonism between gram-positive bacteria. Elife6, 1–24 (2017). https://doi.org/10.7554/eLife.26938 Zhang, 2012, Polymorphic toxin systems: comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics, Biol. Direct, 7, 10.1186/1745-6150-7-18 Tang, 2018, Diverse NADase effector families mediate interbacterial antagonism via the type VI secretion system, J. Biol. Chem., 293, 1504, 10.1074/jbc.RA117.000178 van Nood, 2013, Duodenal infusion of donor feces for recurrent Clostridium difficile, N. Engl. J. Med., 368, 407, 10.1056/NEJMoa1205037 Kelly, 2016, Effect of fecal microbiota transplantation on recurrence in multiply recurrent Clostridium difficile infection: a randomized trial, Ann. Intern. Med., 165, 609, 10.7326/M16-0271 Caballero, 2017, Cooperating commensals restore colonization resistance to vancomycin-resistant Enterococcus faecium, Cell Host Microbe, 21, 592, 10.1016/j.chom.2017.04.002 Becattini, 2017, Commensal microbes provide first line defense against Listeria monocytogenes infection, J. Exp. Med, 214, 1973, 10.1084/jem.20170495 Brugiroux, 2016, Genome-guided design of a defined mouse microbiota that confers colonization resistance against Salmonella enterica serovar Typhimurium, Nat. Microbiol., 2, 16215, 10.1038/nmicrobiol.2016.215 Ubeda, 2013, Intestinal microbiota containing Barnesiella species cures vancomycin-resistant Enterococcus faecium colonization, Infect. Immun., 81, 965, 10.1128/IAI.01197-12 Lawley, 2012, Targeted restoration of the intestinal microbiota with a simple, defined bacteriotherapy resolves relapsing Clostridium difficile disease in mice, PLoS Pathog., 8, e1002995, 10.1371/journal.ppat.1002995 Kim, 2017, The intestinal microbiota: antibiotics, colonization resistance, and enteric pathogens, Immunol. Rev., 279, 90, 10.1111/imr.12563 Lam, 2014, Intraspecies competition for niches in the distal gut dictate transmission during persistent Salmonella infection, PLoS Pathog., 10, e1004527, 10.1371/journal.ppat.1004527 Nedialkova, 2014, Inflammation fuels colicin Ib-dependent competition of Salmonella serovar TyphimuriumE. coli in enterobacterial blooms, PLoS Pathog., 10, e1003844, 10.1371/journal.ppat.1003844 Smajs, 2010, Bacteriocin synthesis in uropathogenic and commensal Escherichia coli: colicin E1 is a potential virulence factor, BMC Microbiol, 10, 288, 10.1186/1471-2180-10-288 Quereda, 2016, Bacteriocin from epidemic Listeria strains alters the host intestinal microbiota to favor infection, Proc. Natl. Acad. Sci. USA, 113, 5706, 10.1073/pnas.1523899113 Quereda, J. J. et al. Listeriolysin S is a streptolysin S-like virulence factor that targets exclusively prokaryotic cells in vivo. MBio8, 1–15 (2017). https://doi.org/10.1128/mBio.00259-17 Fu, 2013, Tn-Seq analysis of Vibrio cholerae intestinal colonization reveals a role for T6SS-mediated antibacterial activity in the host, Cell Host Microbe, 14, 652, 10.1016/j.chom.2013.11.001 LeRoux, M. et al. Kin cell lysis is a danger signal that activates antibacterial pathways of Pseudomonas aeruginosa. Elife4, 1–25 (2015). https://doi.org/10.7554/eLife.05701 Sana, 2016, Salmonella Typhimurium utilizes a T6SS-mediated antibacterial weapon to establish in the host gut, Proc. Natl. Acad. Sci. USA, 113, E5044, 10.1073/pnas.1608858113 LaCourse, 2018, Conditional toxicity and synergy drive diversity among antibacterial effectors, Nature Microbiology, 3, 440, 10.1038/s41564-018-0113-y Bachmann, 2015, Bile salts modulate the mucin-activated type VI secretion system of pandemic Vibrio cholerae, PLoS Negl. Trop. Dis., 9, e0004031, 10.1371/journal.pntd.0004031 Lupp, 2007, Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae, Cell Host Microbe, 2, 204, 10.1016/j.chom.2007.08.002 Stecher, 2007, Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota, PLoS Biol., 5, 2177, 10.1371/journal.pbio.0050244 Palmer, 1988, Vascular endothelial cells synthesize nitric oxide from l-arginine, Nature, 333, 664, 10.1038/333664a0 Rigby, 2012, Neutrophils in innate host defense against Staphylococcus aureus infections, Semin. Immunopathol., 34, 237, 10.1007/s00281-011-0295-3 Fang, 1997, Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity, J. Clin. Invest., 99, 2818, 10.1172/JCI119473 Winter, 2010, Gut inflammation provides a respiratory electron acceptor for Salmonella, Nature, 467, 426, 10.1038/nature09415 Furne, 2001, Oxidation of hydrogen sulfide and methanethiol to thiosulfate by rat tissues: a specialized function of the colonic mucosa, Biochem. Pharmacol., 62, 255, 10.1016/S0006-2952(01)00657-8 Thiennimitr, 2011, Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota, Proc. Natl. Acad. Sci. USA, 108, 17480, 10.1073/pnas.1107857108 Price-Carter, 2001, The alternative electron acceptor tetrathionate supports B12-dependent anaerobic growth of Salmonella enterica serovar typhimurium on ethanolamine or 1,2-propanediol, J. Bacteriol., 183, 2463, 10.1128/JB.183.8.2463-2475.2001 Winter, 2013, Host-derived nitrate boosts growth of E. coli in the inflamed gut, Science, 339, 708, 10.1126/science.1232467 Lundberg, 1994, Greatly increased luminal nitric oxide in ulcerative colitis, Lancet, 344, 1673, 10.1016/S0140-6736(94)90460-X Iobbi-Nivol, 2013, Molybdenum enzymes, their maturation and molybdenum cofactor biosynthesis in Escherichia coli, Biochim. Biophys. Acta, 1827, 1086, 10.1016/j.bbabio.2012.11.007 Spees, A. M. et al. Streptomycin-induced inflammation enhances Escherichia coli gut colonization through nitrate respiration. MBio.4, 1–10 (2013). https://doi.org/10.1128/mBio.00430-13 Rivera-Chavez, 2013, Salmonella uses energy taxis to benefit from intestinal inflammation, PLoS Pathog., 9, e1003267, 10.1371/journal.ppat.1003267 Rivera-Chavez, F. et al. Energy taxis toward host-derived nitrate supports a Salmonella pathogenicity island 1-independent mechanism of invasion. MBio7, 1–11 (2016). https://doi.org/10.1128/mBio.00960-16 Zhu, 2018, Precision editing of the gut microbiota ameliorates colitis, Nature, 553, 208, 10.1038/nature25172 Faber, 2016, Host-mediated sugar oxidation promotes post-antibiotic pathogen expansion, Nature, 534, 697, 10.1038/nature18597 Borisov, 2011, The cytochrome bd respiratory oxygen reductases, Biochim. Biophys. Acta, 1807, 1398, 10.1016/j.bbabio.2011.06.016 Lopez, 2016, Virulence factors enhance Citrobacter rodentium expansion through aerobic respiration, Science, 353, 1249, 10.1126/science.aag3042 Faber, 2017, Respiration of microbiota-derived 1,2-propanediol drives Salmonella expansion during colitis, PLoS Pathog., 13, e1006129, 10.1371/journal.ppat.1006129 Ng, 2013, Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens, Nature, 502, 96, 10.1038/nature12503 Ferreyra, 2014, Gut microbiota-produced succinate promotes C. difficile infection after antibiotic treatment or motility disturbance, Cell Host Microbe, 16, 770, 10.1016/j.chom.2014.11.003 Pham, 2014, Pathogens' exploitation of the intestinal food web, Cell Host Microbe, 16, 703, 10.1016/j.chom.2014.11.012 Curtis, 2014, The gut commensal Bacteroides thetaiotaomicron exacerbates enteric infection through modification of the metabolic landscape, Cell Host Microbe, 16, 759, 10.1016/j.chom.2014.11.005 Vimr, 2004, Diversity of microbial sialic acid metabolism, Microbiol Mol. Biol. Rev., 68, 132, 10.1128/MMBR.68.1.132-153.2004 Spiga, 2017, An oxidative central metabolism enables Salmonella to utilize microbiota-derived succinate, Cell Host Microbe, 22, 291, 10.1016/j.chom.2017.07.018 Maier, 2013, Microbiota-derived hydrogen fuels Salmonella typhimurium invasion of the gut ecosystem, Cell Host Microbe, 14, 641, 10.1016/j.chom.2013.11.002 Becker, 2003, Fucose: biosynthesis and biological function in mammals, Glycobiology, 13, 41R, 10.1093/glycob/cwg054 Pickard, 2014, Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness, Nature, 514, 638, 10.1038/nature13823 Hooper, 1999, A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem, Proc. Natl. Acad. Sci. USA, 96, 9833, 10.1073/pnas.96.17.9833 Chudnovskiy, 2016, Host−protozoan interactions protect from mucosal infections through activation of the inflammasome, Cell, 167, 444, 10.1016/j.cell.2016.08.076 Howitt, 2016, Tuft cells, taste-chemosensory cells, orchestrate parasite type 2 immunity in the gut, Science, 351, 1329, 10.1126/science.aaf1648 Escalante, 2016, The common mouse protozoa Tritrichomonas muris alters mucosal T cell homeostasis and colitis susceptibility, J. Exp. Med, 213, 2841, 10.1084/jem.20161776 Carding, 2017, Review article: the human intestinal virome in health and disease, Aliment Pharmacol. Ther., 46, 800, 10.1111/apt.14280 Lusiak-Szelachowska, 2017, Bacteriophages in the gastrointestinal tract and their implications, Gut Pathog., 9, 10.1186/s13099-017-0196-7 Tropini, 2017, The gut microbiome: connecting spatial organization to function, Cell Host Microbe, 21, 433, 10.1016/j.chom.2017.03.010 Caballero, 2015, Distinct but spatially overlapping intestinal niches for vancomycin-resistant Enterococcus faecium and Carbapenem-resistant Klebsiella pneumoniae, PLoS Pathog., 11, e1005132, 10.1371/journal.ppat.1005132 Whitaker, 2017, Tunable expression tools enable single-cell strain distinction in the gut microbiome, Cell, 169, 538, 10.1016/j.cell.2017.03.041 Earle, 2015, Quantitative imaging of gut microbiota spatial organization, Cell Host Microbe, 18, 478, 10.1016/j.chom.2015.09.002 Heap, 2010, The ClosTron: mutagenesis in Clostridium refined and streamlined, J. Microbiol Methods, 80, 49, 10.1016/j.mimet.2009.10.018 Heap, 2007, The ClosTron: a universal gene knock-out system for the genus Clostridium, J. Microbiol Methods, 70, 452, 10.1016/j.mimet.2007.05.021 Dodd, 2017, A gut bacterial pathway metabolizes aromatic amino acids into nine circulating metabolites, Nature, 551, 648, 10.1038/nature24661 Guo, 2017, Discovery of reactive microbiota-derived metabolites that inhibit host proteases, Cell, 168, 517, 10.1016/j.cell.2016.12.021 Lim, 2017, Engineered regulatory systems modulate gene expression of human commensals in the gut, Cell, 169, 547, 10.1016/j.cell.2017.03.045