Advanced search
Publication Cover
Gut Microbes Volume 16, 2024 - Issue 1
Submit an article Journal homepage
2,513
Views
0
CrossRef citations to date
0
Altmetric
Review

Microbial collaborations and conflicts: unraveling interactions in the gut ecosystem

Shuang Wanga Genomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical University, Harbin, China;b Department of Biopharmaceutical Sciences (State-Province Key Laboratories of Biomedicine-Pharmaceutics of China), College of Pharmacy, Harbin Medical University, Harbin, China;c National Key Laboratory of Frigid Zone Cardiovascular Diseases (NKLFZCD) College of Pharmacy, Harbin Medical University, Harbin, ChinaView further author information
,
Lingyi Mua Genomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical University, Harbin, ChinaView further author information
,
Chong Yua Genomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical University, Harbin, China;c National Key Laboratory of Frigid Zone Cardiovascular Diseases (NKLFZCD) College of Pharmacy, Harbin Medical University, Harbin, China;d Harbin Medical University-University of Calgary Cumming School of Medicine Centre for Infection and Genomics, Harbin Medical University, Harbin, ChinaView further author information
,
Yuting Hea Genomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical University, Harbin, China;c National Key Laboratory of Frigid Zone Cardiovascular Diseases (NKLFZCD) College of Pharmacy, Harbin Medical University, Harbin, China;d Harbin Medical University-University of Calgary Cumming School of Medicine Centre for Infection and Genomics, Harbin Medical University, Harbin, ChinaView further author information
,
Xinliang Hua Genomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical University, Harbin, China;c National Key Laboratory of Frigid Zone Cardiovascular Diseases (NKLFZCD) College of Pharmacy, Harbin Medical University, Harbin, China;d Harbin Medical University-University of Calgary Cumming School of Medicine Centre for Infection and Genomics, Harbin Medical University, Harbin, ChinaView further author information
,
Yanlei Jiaoa Genomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical University, Harbin, China;c National Key Laboratory of Frigid Zone Cardiovascular Diseases (NKLFZCD) College of Pharmacy, Harbin Medical University, Harbin, China;d Harbin Medical University-University of Calgary Cumming School of Medicine Centre for Infection and Genomics, Harbin Medical University, Harbin, ChinaView further author information
,
Ziqiong Xua Genomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical University, Harbin, China;c National Key Laboratory of Frigid Zone Cardiovascular Diseases (NKLFZCD) College of Pharmacy, Harbin Medical University, Harbin, China;d Harbin Medical University-University of Calgary Cumming School of Medicine Centre for Infection and Genomics, Harbin Medical University, Harbin, ChinaView further author information
,
Shaohui Youa Genomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical University, Harbin, China;c National Key Laboratory of Frigid Zone Cardiovascular Diseases (NKLFZCD) College of Pharmacy, Harbin Medical University, Harbin, China;d Harbin Medical University-University of Calgary Cumming School of Medicine Centre for Infection and Genomics, Harbin Medical University, Harbin, ChinaView further author information
,
Shu-Lin Liua Genomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical University, Harbin, China;c National Key Laboratory of Frigid Zone Cardiovascular Diseases (NKLFZCD) College of Pharmacy, Harbin Medical University, Harbin, China;d Harbin Medical University-University of Calgary Cumming School of Medicine Centre for Infection and Genomics, Harbin Medical University, Harbin, ChinaCorrespondence[email protected]
View further author information
&
Hongxia Baoa Genomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical University, Harbin, China;c National Key Laboratory of Frigid Zone Cardiovascular Diseases (NKLFZCD) College of Pharmacy, Harbin Medical University, Harbin, China;d Harbin Medical University-University of Calgary Cumming School of Medicine Centre for Infection and Genomics, Harbin Medical University, Harbin, ChinaCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0001-5026-5777View further author information
ORCID Icon show all
Article: 2296603 | Received 04 Sep 2023, Accepted 14 Dec 2023, Published online: 27 Dec 2023

References

  • Lynch SV, Pedersen O, Phimister EG. The human intestinal microbiome in health and disease. N Engl J Med. 2016;375(24):2369–18. doi:10.1056/NEJMra1600266.
  • Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Sci. 2005;307(5717):1915–1920. doi:10.1126/science.1104816.
  • Marchesi JR. Prokaryotic and eukaryotic diversity of the human gut. Adv Appl Microbiol. 2010;72:43–62.
  • Dominguez-Bello MG, Godoy-Vitorino F, Knight R, Blaser MJ. Role of the microbiome in human development. Gut. 2019;68(6):1108–1114. doi:10.1136/gutjnl-2018-317503.
  • Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordon JI, Relman DA, Fraser-Liggett CM, Nelson KE. Metagenomic analysis of the human distal gut microbiome. Sci. 2006;312(5778):1355–1359. doi:10.1126/science.1124234.
  • Rajilic-Stojanovic M, de Vos WM. The first 1000 cultured species of the human gastrointestinal microbiota. FEMS Microbiol Rev. 2014;38(5):996–1047. doi:10.1111/1574-6976.12075.
  • Korpela K, Costea P, Coelho LP, Kandels-Lewis S, Willemsen G, Boomsma DI, Segata N, Bork P. Selective maternal seeding and environment shape the human gut microbiome. Genome Res. 2018;28(4):561–568. doi:10.1101/gr.233940.117.
  • Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486(7402):222–227. doi:10.1038/nature11053.
  • Stewart CJ, Ajami NJ, O’Brien JL, Hutchinson DS, Smith DP, Wong MC, Ross MC, Lloyd RE, Doddapaneni H, Metcalf GA, et al. Temporal development of the gut microbiome in early childhood from the TEDDY study. Nature. 2018;562(7728):583–588. doi:10.1038/s41586-018-0617-x.
  • Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf H, Goodman AL, Clemente JC, Knight R, Heath AC, Leibel RL, et al. The long-term stability of the human gut microbiota. Science. 2013;341(6141):1237439. doi:10.1126/science.1237439.
  • Machado D, Maistrenko OM, Andrejev S, Kim Y, Bork P, Patil KR, Patil KR. Polarization of microbial communities between competitive and cooperative metabolism. Nat Ecol Evol. 2021;5(2):195–203. doi:10.1038/s41559-020-01353-4.
  • Meredith HR, Srimani JK, Lee AJ, Lopatkin AJ, You L. Collective antibiotic tolerance: mechanisms, dynamics and intervention. Nat Chem Biol. 2015;11(3):182–188. doi:10.1038/nchembio.1754.
  • Bauer MA, Kainz K, Carmona-Gutierrez D, Madeo F. Microbial wars: competition in ecological niches and within the microbiome. Microb Cell. 2018;5(5):215–219. doi:10.15698/mic2018.05.628.
  • Ghoul M, Mitri S. The ecology and evolution of microbial competition. Trends Microbiol. 2016;24(10):833–845. doi:10.1016/j.tim.2016.06.011.
  • Freilich S, Zarecki R, Eilam O, Segal ES, Henry CS, Kupiec M, Gophna U, Sharan R, Ruppin E. Competitive and cooperative metabolic interactions in bacterial communities. Nat Commun. 2011;2(1):589. doi:10.1038/ncomms1597.
  • Rakoff-Nahoum S, Foster KR, Comstock LE. The evolution of cooperation within the gut microbiota. Nature. 2016;533(7602):255–259. doi:10.1038/nature17626.
  • Cornforth DM, Foster KR. Competition sensing: the social side of bacterial stress responses. Nat Rev Microbiol. 2013;11(4):285–293. doi:10.1038/nrmicro2977.
  • Green ER, Mecsas J, Kudva IT. Bacterial secretion systems: an overview. Microbiol Spectr. 2016;4(1). doi:10.1128/microbiolspec.VMBF-0012-2015.
  • Grossman AS, Mauer TJ, Forest KT, Goodrich-Blair H. A widespread bacterial secretion system with diverse substrates. mBio. 2021;12(4):e0195621. doi:10.1128/mBio.01956-21.
  • Gorasia DG, Veith PD, Reynolds EC. The type IX secretion system: advances in structure, function and organisation. Microorgan. 2020;8(8):1173. doi:10.3390/microorganisms8081173.
  • Palmer T, Finney AJ, Saha CK, Atkinson GC, Sargent F. A holin/peptidoglycan hydrolase-dependent protein secretion system. Mol Microbiol. 2021;115(3):345–355. doi:10.1111/mmi.14599.
  • Bao H, Wang S, Zhao JH, Liu SL. Salmonella secretion systems: differential roles in pathogen-host interactions. Microbiol Res. 2020;241:126591. doi:10.1016/j.micres.2020.126591.
  • Crisan CV, Hammer BK. The vibrio cholerae type VI secretion system: toxins, regulators and consequences. Environ Microbiol. 2020;22(10):4112–4122. doi:10.1111/1462-2920.14976.
  • Costa TR, Felisberto-Rodrigues C, Meir A, Prevost MS, Redzej A, Trokter M, Waksman G. Secretion systems in gram-negative bacteria: structural and mechanistic insights. Nat Rev Microbiol. 2015;13(6):343–359. doi:10.1038/nrmicro3456.
  • Tseng TT, Tyler BM, Setubal JC. Protein secretion systems in bacterial-host associations, and their description in the gene ontology. BMC Microbiol. 2009;99(Suppl S1):S2. doi:10.1186/1471-2180-9-S1-S2.
  • Coulthurst S. The type VI secretion system: a versatile bacterial weapon. Microbiol. 2019;165(5):503–515. doi:10.1099/mic.0.000789.
  • Bingle LE, Bailey CM, Pallen MJ. Type VI secretion: a beginner’s guide. Curr Opin Microbiol. 2008;11(1):3–8. doi:10.1016/j.mib.2008.01.006.
  • Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W, Mougous JD. Type VI secretion delivers bacteriolytic effectors to target cells. Nature. 2011;475(7356):343–347. doi:10.1038/nature10244.
  • Wexler AG, Bao Y, Whitney JC, Bobay LM, Xavier JB, Schofield WB, Barry NA, Russell AB, Tran BQ, Goo YA, et al. Human symbionts inject and neutralize antibacterial toxins to persist in the gut. Proc Natl Acad Sci USA. 2016;113(13):3639–3644. doi:10.1073/pnas.1525637113.
  • Coyne MJ, Roelofs KG, Comstock LE. Type VI secretion systems of human gut bacteroidales segregate into three genetic architectures, two of which are contained on mobile genetic elements. Bmc Genom. 2016;17(1):58. doi:10.1186/s12864-016-2377-z.
  • Coyne MJ, Zitomersky NL, McGuire AM, Earl AM, Comstock LE, Mekalanos J. Evidence of extensive DNA transfer between bacteroidales species within the human gut. mBio. 2014;5(3):e01305–01314. doi:10.1128/mBio.01305-14.
  • Coyne MJ, Comstock LE, Sandkvist M, Cascales E, Christie PJ. Type VI secretion systems and the gut microbiota. Microbiol Spectr. 2019;7(2). doi:10.1128/microbiolspec.PSIB-0009-2018.
  • Verster AJ, Ross BD, Radey MC, Bao Y, Goodman AL, Mougous JD, Borenstein E. The landscape of type VI secretion across human gut microbiomes reveals its role in community composition. Cell Host & Microbe. 2017;22(3):411–419 e414. doi:10.1016/j.chom.2017.08.010.
  • Chatzidaki-Livanis M, Geva-Zatorsky N, Comstock LE. Bacteroides fragilis type VI secretion systems use novel effector and immunity proteins to antagonize human gut Bacteroidales species. Proc Natl Acad Sci U S A. 2016;113(13):3627–3632. doi:10.1073/pnas.1522510113.
  • Robitaille S, Simmons EL, Verster AJ, McClure EA, Royce DB, Trus E, Swartz K, Schultz D, Nadell CD, Ross BD. Community composition and the environment modulate the population dynamics of type VI secretion in human gut bacteria. Nat Ecol Evol. 2023;7(12):2092–2107.
  • Garcia-Bayona L, Coyne MJ, Comstock LE, Blokesch M. Mobile type VI secretion system loci of the gut bacteroidales display extensive intra-ecosystem transfer, multi-species spread and geographical clustering. PLoS Genet. 2021;17(4):e1009541. doi:10.1371/journal.pgen.1009541.
  • Bao H, Coyne MJ, Garcia-Bayona L, Comstock LE, O’Toole G. Analysis of effector and immunity proteins of the GA2 type VI secretion systems of gut bacteroidales. J Bacteriol. 2022;204(7):e0012222. doi:10.1128/jb.00122-22.
  • Sheahan ML, Coyne MJ, Flores K, Garcia-Bayona L, Chatzidaki-Livanis M, Sundararajan A, Holst AQ, Barquera B, Comstock LE. A ubiquitous mobile genetic element disarms a bacterial antagonist of the gut microbiota. bioRxiv. 2023.
  • Ross BD, Verster AJ, Radey MC, Schmidtke DT, Pope CE, Hoffman LR, Hajjar AM, Peterson SB, Borenstein E, Mougous JD. Human gut bacteria contain acquired interbacterial defence systems. Nature. 2019;575(7781):224–228. doi:10.1038/s41586-019-1708-z.
  • Ahrodia T, Das S, Bakshi S, Das B. Structure, functions, and diversity of the healthy human microbiome. Prog Mol Biol Transl Sci. 2022;191:53–82.
  • Tenaillon O, Skurnik D, Picard B, Denamur E. The population genetics of commensal Escherichia coli. Nat Rev Microbiol. 2010;8(3):207–217. doi:10.1038/nrmicro2298.
  • Ma J, Bao Y, Sun M, Dong W, Pan Z, Zhang W, Lu C, Yao H, McCormick BA. Two functional type VI secretion systems in avian pathogenic Escherichia coli are involved in different pathogenic pathways. Infect Immun. 2014;82(9):3867–3879. doi:10.1128/IAI.01769-14.
  • Brunet YR, Espinosa L, Harchouni S, Mignot T, Cascales E. Imaging type VI secretion-mediated bacterial killing. Cell Rep. 2013;3(1):36–41. doi:10.1016/j.celrep.2012.11.027.
  • Serapio-Palacios A, Woodward SE, Vogt SL, Deng W, Creus-Cuadros A, Huus KE, Cirstea M, Gerrie M, Barcik W, Yu H, et al. Type VI secretion systems of pathogenic and commensal bacteria mediate niche occupancy in the gut. Cell Rep. 2022;39(4):110731. doi:10.1016/j.celrep.2022.110731.
  • Hecht AL, Casterline BW, Earley ZM, Goo YA, Goodlett DR, Bubeck Wardenburg J. Strain competition restricts colonization of an enteric pathogen and prevents colitis. EMBO Rep. 2016;17(9):1281–1291. doi:10.15252/embr.201642282.
  • Mahairas GG, Sabo PJ, Hickey MJ, Singh DC, Stover CK. Molecular analysis of genetic differences between mycobacterium bovis BCG and virulent M. bovis. J Bacteriol. 1996;178(5):1274–1282. doi:10.1128/jb.178.5.1274-1282.1996.
  • Abdallah AM, Gey van Pittius NC, Champion PA, Cox J, Luirink J, Vandenbroucke-Grauls CM, Appelmelk BJ, Bitter W. Type VII secretion–mycobacteria show the way. Nat Rev Microbiol. 2007;5(11):883–891. doi:10.1038/nrmicro1773.
  • Bowman L, Palmer T. The type VII secretion system of staphylococcus. Annu Rev Microbiol. 2021;75(1):471–494. doi:10.1146/annurev-micro-012721-123600.
  • Pallen MJ. The ESAT-6/WXG100 superfamily – and a new gram-positive secretion system? Trends Microbiol. 2002;10(5):209–212. doi:10.1016/S0966-842X(02)02345-4.
  • Bottai D, Groschel MI, Brosch R. Type VII secretion systems in gram-positive bacteria. Curr Top Microbiol Immunol. 2017;404:235–265.
  • Unnikrishnan M, Constantinidou C, Palmer T, Pallen MJ. The enigmatic Esx proteins: looking beyond mycobacteria. Trends Microbiol. 2017;25(3):192–204. doi:10.1016/j.tim.2016.11.004.
  • Bowran K, Palmer T. Extreme genetic diversity in the type VII secretion system of listeria monocytogenes suggests a role in bacterial antagonism. Microbiol. 2021;167(3). doi:10.1099/mic.0.001034.
  • Bunduc CM, Bitter W, Houben ENG. Structure and function of the mycobacterial type VII secretion systems. Annu Rev Microbiol. 2020;74(1):315–335. doi:10.1146/annurev-micro-012420-081657.
  • Ohr RJ, Anderson M, Shi M, Schneewind O, Missiakas D, Silhavy TJ. EssD, a nuclease effector of the staphylococcus aureus ESS pathway. J Bacteriol. 2017;199(1). doi:10.1128/JB.00528-16.
  • Cao Z, Casabona MG, Kneuper H, Chalmers JD, Palmer T. The type VII secretion system of staphylococcus aureus secretes a nuclease toxin that targets competitor bacteria. Nature Microbiol. 2016;2(1):16183. doi:10.1038/nmicrobiol.2016.183.
  • Ulhuq FR, Gomes MC, Duggan GM, Guo M, Mendonca C, Buchanan G, Chalmers JD, Cao Z, Kneuper H, Murdoch S, et al. A membrane-depolarizing toxin substrate of the staphylococcus aureus type VII secretion system mediates intraspecies competition. Proc Natl Acad Sci USA. 2020;117(34):20836–20847. doi:10.1073/pnas.2006110117.
  • Whitney JC, Peterson SB, Kim J, Pazos M, Verster AJ, Radey MC, Kulasekara HD, Ching MQ, Bullen NP, Bryant D, et al. A broadly distributed toxin family mediates contact-dependent antagonism between gram-positive bacteria. Elife. 2017;6:6. doi:10.7554/eLife.26938.
  • Holberger LE, Garza-Sanchez F, Lamoureux J, Low DA, Hayes CS. A novel family of toxin/antitoxin proteins in bacillus species. FEBS Lett. 2012;586(2):132–136. doi:10.1016/j.febslet.2011.12.020.
  • Kaundal S, Deep A, Kaur G, Thakur KG. Molecular and biochemical characterization of YeeF/YezG, a polymorphic toxin-immunity protein pair from Bacillus subtilis. Front Microbiol. 2020;11:95. doi:10.3389/fmicb.2020.00095.
  • Tassinari M, Doan T, Bellinzoni M, Chabalier M, Ben-Assaya M, Martinez M, Gaday Q, Alzari PM, Cascales E, Fronzes R, et al. The antibacterial type VII secretion system of bacillus subtilis: structure and interactions of the pseudokinase YukC/EssB. mBio. 2022;13(5):e0013422. doi:10.1128/mbio.00134-22.
  • Baptista C, Barreto HC, Sao-Jose C, Cascales E. High levels of DegU-P activate an esat-6-like secretion system in bacillus subtilis. PLoS ONE. 2013;8(7):e67840. doi:10.1371/journal.pone.0067840.
  • Schulthess B, Bloes DA, Berger-Bachi B. Opposing roles of σB and σB-controlled SpoVG in the global regulation of esxA in staphylococcus aureus. BMC Microbiol. 2012;12(1):17. doi:10.1186/1471-2180-12-17.
  • Chatterjee A, Willett JLE, Nguyen UT, Monogue B, Palmer KL, Dunny GM, Duerkop BA, Hatfull GF. Parallel genomics uncover novel enterococcal-bacteriophage interactions. mBio. 2020;11(2). doi:10.1128/mBio.03120-19.
  • Chatterjee A, Willett JLE, Dunny GM, Duerkop BA, Blokesch M. Phage infection and sub-lethal antibiotic exposure mediate enterococcus faecalis type VII secretion system dependent inhibition of bystander bacteria. PLoS Genet. 2021;17(1):e1009204. doi:10.1371/journal.pgen.1009204.
  • Casabona MG, Kneuper H, Alferes de Lima D, Harkins CP, Zoltner M, Hjerde E, Holden MTG, Palmer T. Haem-iron plays a key role in the regulation of the Ess/type VII secretion system of staphylococcus aureus RN6390. Microbiol (Reading). 2017;163(12):1839–1850. doi:10.1099/mic.0.000579.
  • Boopathi S, Liu D, Jia AQ. Molecular trafficking between bacteria determines the shape of gut microbial community. Gut Microbes. 2021;13(1):1959841. doi:10.1080/19490976.2021.1959841.
  • Heilbronner S, Krismer B, Brotz-Oesterhelt H, Peschel A. The microbiome-shaping roles of bacteriocins. Nat Rev Microbiol. 2021;19(11):726–739. doi:10.1038/s41579-021-00569-w.
  • Cotter PD, Ross RP, Hill C. Bacteriocins - a viable alternative to antibiotics? Nat Rev Microbiol. 2013;11(2):95–105. doi:10.1038/nrmicro2937.
  • Garcia-Bayona L, Comstock LE. Bacterial antagonism in host-associated microbial communities. Science. 2018;361:6408. doi:10.1126/science.aat2456.
  • Sanchez-Hidalgo M, Montalban-Lopez M, Cebrian R, Valdivia E, Martinez-Bueno M, Maqueda M. AS-48 bacteriocin: close to perfection. Cell Mol Life Sci. 2011;68(17):2845–2857. doi:10.1007/s00018-011-0724-4.
  • Zheng J, Ganzle MG, Lin XB, Ruan L, Sun M. Diversity and dynamics of bacteriocins from human microbiome. Environ Microbiol. 2015;17(6):2133–2143. doi:10.1111/1462-2920.12662.
  • Lopetuso LR, Giorgio ME, Saviano A, Scaldaferri F, Gasbarrini A, Cammarota G. Bacteriocins and bacteriophages: therapeutic weapons for gastrointestinal diseases? Int J Mol Sci. 2019;20(1):183. doi:10.3390/ijms20010183.
  • Drissi F, Buffet S, Raoult D, Merhej V. Common occurrence of antibacterial agents in human intestinal microbiota. Front Microbiol. 2015;6:441. doi:10.3389/fmicb.2015.00441.
  • Chatzidaki-Livanis M, Coyne MJ, Comstock LE. An antimicrobial protein of the gut symbiont bacteroides fragilis with a MACPF domain of host immune proteins. Mol Microbiol. 2014;94(6):1361–1374. doi:10.1111/mmi.12839.
  • Roelofs KG, Coyne MJ, Gentyala RR, Chatzidaki-Livanis M, Comstock LE, Huffnagle GB. Bacteroidales secreted antimicrobial proteins target surface molecules necessary for gut colonization and mediate competition in vivo. mBio. 2016;7(4). doi:10.1128/mBio.01055-16.
  • McEneany VL, Coyne MJ, Chatzidaki-Livanis M, Comstock LE. Acquisition of MACPF domain-encoding genes is the main contributor to LPS glycan diversity in gut bacteroides species. ISME J. 2018;12(12):2919–2928. doi:10.1038/s41396-018-0244-4.
  • Shumaker AM, Laclare McEneany V, Coyne MJ, Silver PA, Comstock LE, DiRita VJ. Identification of a fifth antibacterial toxin produced by a single bacteroides fragilis strain. J Bacteriol. 2019;201(8). doi:10.1128/JB.00577-18.
  • Chatzidaki-Livanis M, Coyne MJ, Roelofs KG, Gentyala RR, Caldwell JM, Comstock LE, Mekalanos JJ. Gut symbiont bacteroides fragilis secretes a eukaryotic-like ubiquitin protein that mediates intraspecies antagonism. mBio. 2017;8(6). doi:10.1128/mBio.01902-17.
  • Matano LM, Coyne MJ, Garcia-Bayona L, Comstock LE, Stephen Trent M. Bacteroidetocins target the essential outer membrane protein BamA of bacteroidales symbionts and pathogens. mBio. 2021;12(5):e0228521. doi:10.1128/mBio.02285-21.
  • Coyne MJ, Bechon N, Matano LM, McEneany VL, Chatzidaki-Livanis M, Comstock LE. A family of anti-bacteroidales peptide toxins wide-spread in the human gut microbiota. Nat Commun. 2019;10(1):3460. doi:10.1038/s41467-019-11494-1.
  • Cascales E, Buchanan SK, Duche D, Kleanthous C, Lloubes R, Postle K, Riley M, Slatin S, Cavard D. Colicin biology. Microbiol Mol Biol Rev. 2007;71(1):158–229. doi:10.1128/MMBR.00036-06.
  • Majeed H, Gillor O, Kerr B, Riley MA. Competitive interactions in Escherichia coli populations: the role of bacteriocins. ISME J. 2011;5(1):71–81. doi:10.1038/ismej.2010.90.
  • Smajs D, Weinstock GM. Genetic organization of plasmid ColJs, encoding colicin js activity, immunity, and release genes. J Bacteriol. 2001;183(13):3949–3957. doi:10.1128/JB.183.13.3949-3957.2001.
  • Micenkova L, Bosak J, Kucera J, Hrala M, Dolejsova T, Sedo O, Linke D, Fiser R, Smajs D. Colicin Z, a structurally and functionally novel colicin type that selectively kills enteroinvasive Escherichia coli and shigella strains. Sci Rep. 2019;9(1):11127. doi:10.1038/s41598-019-47488-8.
  • Rendueles O, Beloin C, Latour-Lambert P, Ghigo JM. A new biofilm-associated colicin with increased efficiency against biofilm bacteria. ISME J. 2014;8(6):1275–1288. doi:10.1038/ismej.2013.238.
  • Gillor O, Giladi I, Riley MA. Persistence of colicinogenic Escherichia coli in the mouse gastrointestinal tract. BMC Microbiol. 2009;9(1):165. doi:10.1186/1471-2180-9-165.
  • Nedialkova LP, Denzler R, Koeppel MB, Diehl M, Ring D, Wille T, Gerlach RG, Stecher B, Galán JE. Inflammation fuels colicin Ib-dependent competition of salmonella serovar typhimurium and E. coli in enterobacterial blooms. PLoS Pathog. 2014;10(1):e1003844. doi:10.1371/journal.ppat.1003844.
  • Hancock V, Dahl M, Klemm P. Probiotic Escherichia coli strain Nissle 1917 outcompetes intestinal pathogens during biofilm formation. J Med Microbiol. 2010;59(Pt 4):392–399. doi:10.1099/jmm.0.008672-0.
  • Gordon DM, Riley MA, Pinou T. Pinou T: temporal changes in the frequency of colicinogeny in Escherichia coli from house mice. Microbiol. 1998;144(8):2233–2240. doi:10.1099/00221287-144-8-2233.
  • Gillor O, Vriezen JAC, Riley MA. The role of SOS boxes in enteric bacteriocin regulation. Microbiol. 2008;154(Pt 6):1783–1792. doi:10.1099/mic.0.2007/016139-0.
  • Kirkup BC, Riley MA. Antibiotic-mediated antagonism leads to a bacterial game of rock-paper-scissors in vivo. Nature. 2004;428(6981):412–414. doi:10.1038/nature02429.
  • Rebuffat S. Microcins in action: amazing defence strategies of enterobacteria. Biochem Soc Trans. 2012;40(6):1456–1462. doi:10.1042/BST20120183.
  • Yang SC, Lin CH, Sung CT, Fang JY. Antibacterial activities of bacteriocins: application in foods and pharmaceuticals. Front Microbiol. 2014;5:241. doi:10.3389/fmicb.2014.00241.
  • Sassone-Corsi M, Nuccio SP, Liu H, Hernandez D, Vu CT, Takahashi AA, Edwards RA, Raffatellu M. Microcins mediate competition among Enterobacteriaceae in the inflamed gut. Nature. 2016;540(7632):280–283. doi:10.1038/nature20557.
  • Willey JM, van der Donk WA. Lantibiotics: peptides of diverse structure and function. Annu Rev Microbiol. 2007;61(1):477–501. doi:10.1146/annurev.micro.61.080706.093501.
  • Jozefiak D, Kieronczyk B, Juskiewicz J, Zdunczyk Z, Rawski M, Dlugosz J, Sip A, Hojberg O, Loh G. Dietary nisin modulates the gastrointestinal microbial ecology and enhances growth performance of the broiler chickens. PLoS ONE. 2013;8(12):e85347. doi:10.1371/journal.pone.0085347.
  • Jia Z, Chen A, Bao F, He M, Gao S, Xu J, Zhang X, Niu P, Wang C. Effect of nisin on microbiome-brain-gut axis neurochemicals by Escherichia coli-induced diarrhea in mice. Microb Pathog. 2018;119:65–71. doi:10.1016/j.micpath.2018.04.005.
  • O’Reilly C, Grimaud GM, Coakley M, O’Connor PM, Mathur H, Peterson VL, O’Donovan CM, Lawlor PG, Cotter PD, Stanton C, et al. Modulation of the gut microbiome with nisin. Sci Rep. 2023;13(1):7899. doi:10.1038/s41598-023-34586-x.
  • van Staden DA, Brand AM, Endo A, Dicks LM. Intraperitoneally injected, may have a stabilizing effect on the bacterial population in the gastro-intestinal tract, as determined in a preliminary study with mice as model. Lett Appl Microbiol. 2011;53(2):198–201. doi:10.1111/j.1472-765X.2011.03091.x.
  • Lawrence GW, McCarthy N, Walsh CJ, Kunyoshi TM, Lawton EM, O’Connor PM, Begley M, Cotter PD, Guinane CM. Effect of a bacteriocin-producing Streptococcus salivarius on the pathogen Fusobacterium nucleatum in a model of the human distal colon. Gut Microbes. 2022;14(1):2100203. doi:10.1080/19490976.2022.2100203.
  • Kwok LY, Guo Z, Zhang J, Wang L, Qiao J, Hou Q, Zheng Y, Zhang H. The impact of oral consumption of lactobacillus plantarum P-8 on faecal bacteria revealed by pyrosequencing. Benef Microbes. 2015;6(4):405–413. doi:10.3920/BM2014.0063.
  • Umu OC, Bauerl C, Oostindjer M, Pope PB, Hernandez PE, Perez-Martinez G, Diep DB. The potential of class II bacteriocins to modify gut microbiota to improve host health. PLoS ONE. 2016;11:e0164036.
  • Stubbendieck RM, Straight PD, Margolin W. Multifaceted interfaces of bacterial competition. J Bacteriol. 2016;198(16):2145–2155. doi:10.1128/JB.00275-16.
  • Venturelli OS, Carr AC, Fisher G, Hsu RH, Lau R, Bowen BP, Hromada S, Northen T, Arkin AP. Deciphering microbial interactions in synthetic human gut microbiome communities. Mol Syst Biol. 2018;14(6):e8157. doi:10.15252/msb.20178157.
  • Coyte KZ, Rakoff-Nahoum S. Understanding competition and cooperation within the mammalian gut microbiome. Curr Biol. 2019;29(11):R538–R544. doi:10.1016/j.cub.2019.04.017.
  • Levy R, Borenstein E. Metabolic modeling of species interaction in the human microbiome elucidates community-level assembly rules. Proc Natl Acad Sci USA. 2013;110(31):12804–12809. doi:10.1073/pnas.1300926110.
  • Biggs MB, Medlock GL, Moutinho TJ, Lees HJ, Swann JR, Kolling GL, Papin JA. Systems-level metabolism of the altered schaedler flora, a complete gut microbiota. ISME J. 2017;11(2):426–438. doi:10.1038/ismej.2016.130.
  • Xu J, Mahowald MA, Ley RE, Lozupone CA, Hamady M, Martens EC, Henrissat B, Coutinho PM, Minx P, Latreille P, et al. Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol. 2007;5(7):e156. doi:10.1371/journal.pbio.0050156.
  • Rakoff-Nahoum S, Coyne MJ, Comstock LE. An ecological network of polysaccharide utilization among human intestinal symbionts. Curr Biol. 2014;24(1):40–49. doi:10.1016/j.cub.2013.10.077.
  • Sonnenburg ED, Zheng H, Joglekar P, Higginbottom SK, Firbank SJ, Bolam DN, Sonnenburg JL. Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations. Cell. 2010;141(7):1241–1252. doi:10.1016/j.cell.2010.05.005.
  • Leth ML, Ejby M, Workman C, Ewald DA, Pedersen SS, Sternberg C, Bahl MI, Licht TR, Aachmann FL, Westereng B, et al. Differential bacterial capture and transport preferences facilitate co-growth on dietary xylan in the human gut. Nature Microbiol. 2018;3(5):570–580. doi:10.1038/s41564-018-0132-8.
  • Holdridge EM, Cuellar-Gempeler C, terHorst CP. A shift from exploitation to interference competition with increasing density affects population and community dynamics. Ecol Evol. 2016;6(15):5333–5341. doi:10.1002/ece3.2284.
  • Foster KR, Bell T. Bell T: competition, not cooperation, dominates interactions among culturable microbial species. Curr Biol. 2012;22(19):1845–1850. doi:10.1016/j.cub.2012.08.005.
  • Hibbing ME, Fuqua C, Parsek MR, Peterson SB. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol. 2010;8(1):15–25. doi:10.1038/nrmicro2259.
  • Zelezniak A, Andrejev S, Ponomarova O, Mende DR, Bork P, Patil KR. Metabolic dependencies drive species co-occurrence in diverse microbial communities. Proc Natl Acad Sci USA. 2015;112(20):6449–6454. doi:10.1073/pnas.1421834112.
  • D’Souza G, Shitut S, Preussger D, Yousif G, Waschina S, Kost C. Ecology and evolution of metabolic cross-feeding interactions in bacteria. Nat Prod Rep. 2018;35(5):455–488. doi:10.1039/C8NP00009C.
  • Little AE, Robinson CJ, Peterson SB, Raffa KF, Handelsman J. Rules of engagement: interspecies interactions that regulate microbial communities. Annu Rev Microbiol. 2008;62(1):375–401. doi:10.1146/annurev.micro.030608.101423.
  • Elias S, Banin E. Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev. 2012;36(5):990–1004. doi:10.1111/j.1574-6976.2012.00325.x.
  • Ziesack M, Gibson T, Oliver JKW, Shumaker AM, Hsu BB, Riglar DT, Giessen TW, DiBenedetto NV, Bry L, Way JC, et al. Engineered interspecies amino acid cross-feeding increases population evenness in a synthetic bacterial consortium. mSystems. 2019;4(4). doi:10.1128/mSystems.00352-19.
  • Ponomarova O, Gabrielli N, Sevin DC, Mulleder M, Zirngibl K, Bulyha K, Andrejev S, Kafkia E, Typas A, Sauer U, et al. Yeast creates a niche for symbiotic lactic acid bacteria through nitrogen overflow. Cell Syst. 2017;5(4):345–357.e6. doi:10.1016/j.cels.2017.09.002.
  • Sokolovskaya OM, Shelton AN, Taga ME. Sharing vitamins: cobamides unveil microbial interactions. Sci. 2020;369(6499):6499. doi:10.1126/science.aba0165.
  • Solden LM, Naas AE, Roux S, Daly RA, Collins WB, Nicora CD, Purvine SO, Hoyt DW, Schuckel J, Jorgensen B, et al. Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem. Nature Microbiol. 2018;3(11):1274–1284. doi:10.1038/s41564-018-0225-4.
  • Kehe J, Ortiz A, Kulesa A, Gore J, Blainey PC, Friedman J. Positive interactions are common among culturable bacteria. Sci Adv. 2021;7(45):eabi7159. doi:10.1126/sciadv.abi7159.
  • Alvarez-Mercado AI, Plaza-Diaz J. Dietary polysaccharides as modulators of the gut microbiota ecosystem: an update on their impact on health. Nutrients. 2022;14(19):4116. doi:10.3390/nu14194116.
  • McKee LS, La Rosa SL, Westereng B, Eijsink VG, Pope PB, Larsbrink J. Polysaccharide degradation by the bacteroidetes: mechanisms and nomenclature. Environ Microbiol Rep. 2021;13(5):559–581. doi:10.1111/1758-2229.12980.
  • Grondin JM, Tamura K, Dejean G, Abbott DW, Brumer H, O’Toole G. Polysaccharide utilization loci: fueling microbial communities. J Bacteriol. 2017;199(15). doi:10.1128/JB.00860-16.
  • Zeybek N, Rastall RA, Buyukkileci AO. Utilization of xylan-type polysaccharides in co-culture fermentations of bifidobacterium and bacteroides species. Carbohydr Polym. 2020;236:116076. doi:10.1016/j.carbpol.2020.116076.
  • Tannock GW, Lawley B, Munro K, Sims IM, Lee J, Butts CA, Roy N, Macfarlane GT. RNA–stable-Isotope probing shows utilization of carbon from inulin by specific bacterial populations in the rat large bowel. Appl Environ Microbiol. 2014;80(7):2240–2247. doi:10.1128/AEM.03799-13.
  • Milani C, Lugli GA, Duranti S, Turroni F, Mancabelli L, Ferrario C, Mangifesta M, Hevia A, Viappiani A, Scholz M, et al. Bifidobacteria exhibit social behavior through carbohydrate resource sharing in the gut. Sci Rep. 2015;5(1):15782. doi:10.1038/srep15782.
  • Turroni F, Milani C, Duranti S, Mahony J, van Sinderen D, Ventura M. Glycan utilization and cross-feeding activities by bifidobacteria. Trends Microbiol. 2018;26(4):339–350. doi:10.1016/j.tim.2017.10.001.
  • Egan M, O’Connell Motherway M, Ventura M, van Sinderen D, Macfarlane GT. Metabolism of sialic acid by bifidobacterium breve UCC2003. Appl Environ Microbiol. 2014;80(14):4414–4426. doi:10.1128/AEM.01114-14.
  • Cheng CC, Duar RM, Lin X, Perez-Munoz ME, Tollenaar S, Oh JH, van Pijkeren JP, Li F, van Sinderen D, Ganzle MG, et al. Ecological importance of cross-feeding of the intermediate metabolite 1,2-propanediol between bacterial gut symbionts. Appl Environ Microbiol. 2020;86(11). doi:10.1128/AEM.00190-20.
  • Belenguer A, Duncan SH, Calder AG, Holtrop G, Louis P, Lobley GE, Flint HJ. Two routes of metabolic cross-feeding between bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl Environ Microbiol. 2006;72(5):3593–3599. doi:10.1128/AEM.72.5.3593-3599.2006.
  • Thebault E, Fontaine C. Stability of ecological communities and the architecture of mutualistic and trophic networks. Science. 2010;329(5993):853–856. doi:10.1126/science.1188321.
  • Rohr RP, Saavedra S, Bascompte J. Ecological networks. On the structural stability of mutualistic systems. Science. 2014;345(6195):1253497. doi:10.1126/science.1253497.
  • Seth EC, Taga ME. Nutrient cross-feeding in the microbial world. Front Microbiol. 2014;5:350. doi:10.3389/fmicb.2014.00350.
  • Riviere A, Gagnon M, Weckx S, Roy D, De Vuyst L, Schloss PD. Mutual cross-feeding interactions between bifidobacterium longum subsp. longum NCC2705 and eubacterium rectale ATCC 33656 explain the bifidogenic and butyrogenic effects of arabinoxylan oligosaccharides. Appl Environ Microbiol. 2015;81(22):7767–7781. doi:10.1128/AEM.02089-15.
  • Faust K, Raes J. Microbial interactions: from networks to models. Nat Rev Microbiol. 2012;10(8):538–550. doi:10.1038/nrmicro2832.
  • Schink B. Synergistic interactions in the microbial world. Antonie Van Leeuwenhoek. 2002;81(1–4):257–261. doi:10.1023/A:1020579004534.
  • Bui TPN, Schols HA, Jonathan M, Stams AJM, de Vos WM, Plugge CM. Mutual metabolic interactions in co-cultures of the intestinal anaerostipes rhamnosivorans with an acetogen, methanogen, or pectin-degrader affecting butyrate production. Front Microbiol. 2019;10:2449. doi:10.3389/fmicb.2019.02449.
  • Samuel BS, Gordon JI. A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proc Natl Acad Sci USA. 2006;103(26):10011–10016. doi:10.1073/pnas.0602187103.
  • Palmer RJ Jr., Kazmerzak K, Hansen MC, Kolenbrander PE, Moore RN. Mutualism versus independence: strategies of mixed-species oral biofilms in vitro using saliva as the sole nutrient source. Infect Immun. 2001;69(9):5794–5804. doi:10.1128/IAI.69.9.5794-5804.2001.
  • Sadiq FA, Wenwei L, Heyndrickx M, Flint S, Wei C, Jianxin Z, Zhang H. Synergistic interactions prevail in multispecies biofilms formed by the human gut microbiota on mucin. FEMS Microbiol Ecol. 2021;97(8). doi:10.1093/femsec/fiab096.
  • Ona L, Giri S, Avermann N, Kreienbaum M, Thormann KM, Kost C. Obligate cross-feeding expands the metabolic niche of bacteria. Nat Ecol Evol. 2021;5(9):1224–1232. doi:10.1038/s41559-021-01505-0.
  • Hoek M, Merks RMH. Emergence of microbial diversity due to cross-feeding interactions in a spatial model of gut microbial metabolism. BMC Syst Biol. 2017;11(1):56. doi:10.1186/s12918-017-0430-4.
  • Mee MT, Collins JJ, Church GM, Wang HH. Syntrophic exchange in synthetic microbial communities. Proc Natl Acad Sci USA. 2014;111(20):E2149–2156. doi:10.1073/pnas.1405641111.
  • Yurtsev EA, Conwill A, Gore J. Oscillatory dynamics in a bacterial cross-protection mutualism. Proc Natl Acad Sci USA. 2016;113(22):6236–6241. doi:10.1073/pnas.1523317113.
  • Pande S, Merker H, Bohl K, Reichelt M, Schuster S, de Figueiredo LF, Kaleta C, Kost C. Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria. ISME J. 2014;8(5):953–962. doi:10.1038/ismej.2013.211.
  • McInnes RS, McCallum GE, Lamberte LE, van Schaik W. Horizontal transfer of antibiotic resistance genes in the human gut microbiome. Curr Opin Microbiol. 2020;53:35–43. doi:10.1016/j.mib.2020.02.002.
  • Lee IPA, Eldakar OT, Gogarten JP, Andam CP. Bacterial cooperation through horizontal gene transfer. Trends Ecol Evol. 2022;37(3):223–232. doi:10.1016/j.tree.2021.11.006.
  • Macfarlane S, Macfarlane GT. Composition and metabolic activities of bacterial biofilms colonizing food residues in the human gut. Appl Environ Microbiol. 2006;72(9):6204–6211. doi:10.1128/AEM.00754-06.
  • Dubois T, Tremblay YDN, Hamiot A, Martin-Verstraete I, Deschamps J, Monot M, Briandet R, Dupuy B. A microbiota-generated bile salt induces biofilm formation in clostridium difficile. NPJ Biofilms Microbio. 2019;5(1):14. doi:10.1038/s41522-019-0087-4.
  • Bechon N, Ghigo JM. Gut biofilms: bacteroides as model symbionts to study biofilm formation by intestinal anaerobes. FEMS Microbiol Rev. 2022;46(2). doi:10.1093/femsre/fuab054.
  • Michalak L, Gaby JC, Lagos L, La Rosa SL, Hvidsten TR, Tetard-Jones C, Willats WGT, Terrapon N, Lombard V, Henrissat B, et al. Microbiota-directed fibre activates both targeted and secondary metabolic shifts in the distal gut. Nat Commun. 2020;11(1):5773. doi:10.1038/s41467-020-19585-0.
  • Toyofuku M, Nomura N, Eberl L. Types and origins of bacterial membrane vesicles. Nat Rev Microbiol. 2019;17(1):13–24. doi:10.1038/s41579-018-0112-2.
  • Schwechheimer C, Kuehn MJ. Outer-membrane vesicles from gram-negative bacteria: biogenesis and functions. Nat Rev Microbiol. 2015;13(10):605–619. doi:10.1038/nrmicro3525.
  • Kaparakis-Liaskos M, Ferrero RL. Immune modulation by bacterial outer membrane vesicles. Nat Rev Immunol. 2015;15(6):375–387. doi:10.1038/nri3837.
  • Zavan L, Bitto N, Kaparakis-Liaskos MJI. History, vesicles dobm: bacterial membrane vesicles. Biogen Funct Applicat. 2020;1:1–21.
  • Dean SN, Leary DH, Sullivan CJ, Oh E, Walper SA. Isolation and characterization of lactobacillus-derived membrane vesicles. Sci Rep. 2019;9(1):877. doi:10.1038/s41598-018-37120-6.
  • Dean SN, Rimmer MA, Turner KB, Phillips DA, Caruana JC, Hervey W, Leary DH, Walper SA. Lactobacillus acidophilus membrane vesicles as a vehicle of bacteriocin delivery. Front Microbiol. 2020;11:710. doi:10.3389/fmicb.2020.00710.
  • Evans AGL, Davey HM, Cookson A, Currinn H, Cooke-Fox G, Stanczyk PJ, Whitworth DE. Predatory activity of myxococcus xanthus outer-membrane vesicles and properties of their hydrolase cargo. Microbiol. 2012;158(Pt 11):2742–2752. doi:10.1099/mic.0.060343-0.
  • Elhenawy W, Debelyy MO, Feldman MF, Whiteley M, Greenberg EP. Preferential packing of acidic glycosidases and proteases into bacteroides outer membrane vesicles. mBio. 2014;5(2):e00909–00914. doi:10.1128/mBio.00909-14.
  • Hickey CA, Kuhn KA, Donermeyer DL, Porter NT, Jin C, Cameron EA, Jung H, Kaiko GE, Wegorzewska M, Malvin NP, et al. Colitogenic bacteroides thetaiotaomicron antigens access host immune cells in a sulfatase-dependent manner via outer membrane vesicles. Cell Host & Microbe. 2015;17(5):672–680. doi:10.1016/j.chom.2015.04.002.
  • Stentz R, Horn N, Cross K, Salt L, Brearley C, Livermore DM, Carding SR. Cephalosporinases associated with outer membrane vesicles released by bacteroides spp. protect gut pathogens and commensals against beta-lactam antibiotics. J Antimicrob Chemother. 2015;70(3):701–709. doi:10.1093/jac/dku466.
  • James C, Dixon R, Talbot L, James SJ, Williams N, Onarinde BA. Assessing the impact of heat treatment of food on antimicrobial resistance genes and their potential uptake by other bacteria—a critical review. Antibiot (Basel). 2021;10(12):1440. doi:10.3390/antibiotics10121440.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.