{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,20]],"date-time":"2026-08-20T15:52:03Z","timestamp":1787241123697,"version":"build-2736575974"},"reference-count":42,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2020,12,3]],"date-time":"2020-12-03T00:00:00Z","timestamp":1606953600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>\n                    <jats:italic>Neisseria gonorrhoeae<\/jats:italic>\n                    infections are a serious global health problem. This organism has developed disturbing levels of antibiotic resistance, resulting in the need for new approaches to prevent and treat gonorrhea. The genus\n                    <jats:italic>Neisseria<\/jats:italic>\n                    also includes several members of the human microbiome that live in close association with an array of microbial partners in a variety of niches. We designed an undergraduate antibiotic discovery project to examine a panel of nonpathogenic\n                    <jats:italic>Neisseria<\/jats:italic>\n                    species for their ability to produce antimicrobial secondary metabolites. Five strains belonging to the\n                    <jats:italic>N. mucosa<\/jats:italic>\n                    species group displayed activity against other\n                    <jats:italic>Neisseria<\/jats:italic>\n                    in delayed antagonism assays; three of these were active against\n                    <jats:italic>N. gonorrhoeae<\/jats:italic>\n                    . The antimicrobial compound secreted by\n                    <jats:italic>N. mucosa<\/jats:italic>\n                    NRL 9300 remained active in the presence of catalase, trypsin, and HEPES buffer, and effectively inhibited a DNA uptake mutant of\n                    <jats:italic>N. gonorrhoeae<\/jats:italic>\n                    . Antimicrobial activity was also retained in an ethyl acetate extract of plate grown\n                    <jats:italic>N. mucosa<\/jats:italic>\n                    NRL 9300. These data suggest\n                    <jats:italic>N. mucosa<\/jats:italic>\n                    produces an antimicrobial secondary metabolite that is distinct from previously described antigonococcal agents. This work also serves as a demonstration project that could easily be adapted to studying other members of the human microbiome in undergraduate settings. We offer the perspective that both introductory and more advanced course-based and apprentice-style antibiotic discovery projects focused on the microbiome have the potential to enrich undergraduate curricula and we describe transferrable techniques and strategies to facilitate project design.\n                  <\/jats:p>","DOI":"10.3389\/fmicb.2020.577762","type":"journal-article","created":{"date-parts":[[2020,12,3]],"date-time":"2020-12-03T03:34:39Z","timestamp":1606966479000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":22,"title":["The Human Microbiome as a Focus of Antibiotic Discovery: Neisseria mucosa Displays Activity Against Neisseria gonorrhoeae"],"prefix":"10.3389","volume":"11","author":[{"given":"Ellen L.","family":"Aho","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jenie M.","family":"Ogle","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna M.","family":"Finck","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2020,12,3]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"1570","DOI":"10.1099\/mic.0.056077-0","article-title":"A genomic approach to bacterial taxonomy: an examination and proposed reclassification of species within the genus Neisseria.","volume":"158","author":"Bennett","year":"2012","journal-title":"Microbiology"},{"key":"B2","doi-asserted-by":"publisher","first-page":"1375","DOI":"10.1128\/JCM.03529-13","article-title":"Identifying Neisseria species by use of the 50S ribosomal protein L6 (rplF) gene.","volume":"52","author":"Bennett","year":"2014","journal-title":"J. Clin. Microbiol."},{"key":"B3","year":"2012","journal-title":"Cephalosporin-Resistant Neisseria Gonorrhoeae Public Health Response Plan."},{"key":"B4","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1008372","article-title":"Commensal Neisseria cinerea impairs Neisseria meningitidis microcolony development and reduces pathogen colonisation of epithelial cells.","volume":"16","author":"Custodio","year":"2020","journal-title":"PLoS Pathog."},{"key":"B5","doi-asserted-by":"publisher","first-page":"1512","DOI":"10.1093\/cid\/civ098","article-title":"Nasal inoculation of the commensal Neisseria lactamica inhibits carriage of Neisseria meningitidis by young adults: a controlled human infection study.","volume":"60","author":"Deasy","year":"2015","journal-title":"Clin. Infect. Dis."},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.1038\/nmicrobiol.2016.70","article-title":"Uncovering oral Neisseria tropism and persistence using metagenomic sequencing.","volume":"1","author":"Donati","year":"2016","journal-title":"Nat. Microbiol."},{"key":"B7","doi-asserted-by":"publisher","DOI":"10.1126\/science.1254766","article-title":"Small molecules from the human microbiota.","volume":"349","author":"Donia","year":"2015","journal-title":"Science"},{"key":"B8","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1002\/bmb.21121","article-title":"Design of a drug discovery course for non-science majors.","volume":"46","author":"Dube","year":"2018","journal-title":"Biochem. Mol. Biol. Educ."},{"key":"B9","doi-asserted-by":"publisher","first-page":"E2875","DOI":"10.1073\/pnas.1409644111","article-title":"Oligotyping analysis of the human oral microbiome.","volume":"111","author":"Eren","year":"2014","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B10","year":"2019","journal-title":"Response Plan to Control and Manage The Threat of Multi- and Extensively Drug-Resistant Gonorrhoeae in Europe \u2013 2019 Update."},{"key":"B11","doi-asserted-by":"publisher","DOI":"10.2807\/1560-7917.ES.2018.23.27.1800323","article-title":"Gonorrhea treatment failure caused by a Neisseria gonorrhoeae strain with combined ceftriaxone and high-level azithromycin resistance, England, February 2018.","volume":"23","author":"Eyre","year":"2018","journal-title":"Euro Surveill."},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2017.00502","article-title":"Vaginal lactobacilli reduce Neisseria gonorrhoeae viability through multiple strategies: an in vitro study.","volume":"7","author":"Foschi","year":"2017","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"B13","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1128\/jmbe.v19i3.1603","article-title":"The PARE Project: a short course-based research project for national surveillance of antibiotic-resistant microbes in environmental samples.","volume":"19","author":"Genn\u00e9-Bacon","year":"2018","journal-title":"J. Microbiol. Biol. Educ."},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.1186\/1476-0711-10-8","article-title":"The role of acidification in the inhibition of Neisseria gonorrhoeae by vaginal lactobacilli during anaerobic growth.","volume":"10","author":"Graver","year":"2011","journal-title":"Ann. Clin. Microbiol. Antimicrob."},{"key":"B15","author":"Hernandez","year":"2018","journal-title":"Tiny Earth: A Research Guide to Studentsourcing Antibiotic Discovery."},{"key":"B16","doi-asserted-by":"publisher","DOI":"10.1093\/femsle\/fnv138","article-title":"Inspiring STEM undergraduates to tackle the AMR crisis.","volume":"362","author":"Hoskisson","year":"2015","journal-title":"FEMS Microbiol. Lett."},{"key":"B17","doi-asserted-by":"publisher","first-page":"994","DOI":"10.1126\/science.1183605","article-title":"A catalog of reference genomes from the human microbiome.","volume":"328","author":"Nelson","year":"2010","journal-title":"Science"},{"key":"B18","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1038\/nature11209","article-title":"A framework for human microbiome research.","volume":"486","year":"2012","journal-title":"Nature"},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.12688\/wellcomeopenres.14826.1","article-title":"Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications.","volume":"3","author":"Jolley","year":"2018","journal-title":"Wellcome Open Res."},{"key":"B20","doi-asserted-by":"publisher","first-page":"335","DOI":"10.1111\/j.1699-0463.1982.tb00128.x","article-title":"Three types of growth inhibition among strains of Neisseria meningitidis isolated from patients in Norway.","volume":"90","author":"Jyssum","year":"1982","journal-title":"Acta Pathol. Microbiol. Immunol. Scand. B"},{"key":"B21","doi-asserted-by":"crossref","first-page":"1274","DOI":"10.1128\/JB.85.6.1274-1279.1963","article-title":"Neisseria gonorrhoeae. I. Virulence genetically linked to clonal variation.","volume":"85","author":"Kellogg","year":"1963","journal-title":"J. Bacteriol."},{"key":"B22","doi-asserted-by":"publisher","first-page":"228","DOI":"10.1016\/j.chom.2019.07.003","article-title":"Commensal Neisseria kill Neisseria gonorrhoeae through a DNA-dependent mechanism.","volume":"26","author":"Kim","year":"2019","journal-title":"Cell Host Microbe"},{"key":"B23","doi-asserted-by":"publisher","first-page":"274","DOI":"10.1136\/jcp.28.4.274","article-title":"Reevaluation of bacteriocinogeny in Neisseria gonorrhoeae.","volume":"28","author":"Knapp","year":"1975","journal-title":"J. Clin. Pathol."},{"key":"B24","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0097279","article-title":"The prevalence of species and strains in the human microbiome: a resource for experimental efforts.","volume":"9","author":"Kraal","year":"2014","journal-title":"PLoS One"},{"key":"B25","doi-asserted-by":"publisher","first-page":"1297","DOI":"10.1099\/mic.0.000086","article-title":"Non-pathogenic Neisseria: members of an abundant, multi-habitat, diverse genus.","volume":"161","author":"Liu","year":"2015","journal-title":"Microbiology"},{"key":"B26","doi-asserted-by":"publisher","first-page":"S12","DOI":"10.1086\/514917","article-title":"Horizontal genetic exchange, evolution, and spread of antibiotic resistance in bacteria.","volume":"27","author":"Maiden","year":"1998","journal-title":"Clin. Infect. Dis."},{"key":"B27","doi-asserted-by":"publisher","first-page":"E791","DOI":"10.1073\/pnas.1522149113","article-title":"Biogeography of a human oral microbiome at the micron scale.","volume":"113","author":"Mark Welch","year":"2016","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2014.00568","article-title":"Dynamics of tongue microbial communities with single-nucleotide resolution using oligotyping.","volume":"5","author":"Mark Welch","year":"2014","journal-title":"Front. Microbiol."},{"key":"B29","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0011835","article-title":"Genome sequencing reveals widespread virulence gene exchange among human Neisseria species.","volume":"5","author":"Marri","year":"2010","journal-title":"PLoS One"},{"key":"B30","doi-asserted-by":"publisher","first-page":"725","DOI":"10.1016\/j.chom.2018.05.013","article-title":"Accessing bioactive natural products from the human microbiome.","volume":"23","author":"Milshteyn","year":"2018","journal-title":"Cell Host Microbe"},{"key":"B31","doi-asserted-by":"publisher","first-page":"548","DOI":"10.2471\/BLT.18.228486","article-title":"Chlamydia, gonorrhea, trichomoniasis and syphilis: global prevalence and incidence estimates, 2016.","volume":"97","author":"Rowley","year":"2019","journal-title":"Bull. World Health Organ."},{"key":"B32","doi-asserted-by":"publisher","DOI":"10.1093\/femspd\/ftv013","article-title":"Bacteriocins and other bioactive substances of probiotic lactobacilli as biological weapons against Neisseria gonorrhoeae.","volume":"73","author":"Ru\u00edz","year":"2015","journal-title":"Pathog. Dis."},{"key":"B33","first-page":"59","article-title":"An authentic course-based research experience in antibiotic resistance and microbial genomics.","volume":"9","author":"Smyth","year":"2017","journal-title":"Sci. Educ. Civic Engag."},{"key":"B34","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1007\/BF00182388","article-title":"Role of interspecies transfer of chromosomal genes in the evolution of penicillin resistance in pathogenic and commensal Neisseria species.","volume":"34","author":"Spratt","year":"1992","journal-title":"J. Mol. Evol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"7169","DOI":"10.1128\/iai.70.12.7169-7171.2002","article-title":"Inhibition of Neisseria gonorrhoeae by Lactobacillus species that are commonly isolated from the female genital tract.","volume":"70","author":"St. Amant","year":"2002","journal-title":"Infect. Immun."},{"key":"B36","doi-asserted-by":"publisher","DOI":"10.1038\/s41572-019-0128-6","article-title":"Gonorrhoea.","volume":"5","author":"Unemo","year":"2019","journal-title":"Nat. Rev. Dis. Primers"},{"key":"B37","doi-asserted-by":"publisher","first-page":"5619","DOI":"10.1128\/jb.184.20.5619-5624.2002","article-title":"Overexpression of the MtrC-MtrD-MtrE efflux pump due to an mtrR mutation is required for chromosomally mediated penicillin resistance in Neisseria gonorrhoeae.","volume":"184","author":"Veal","year":"2002","journal-title":"J. Bacteriol."},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.1093\/femspd\/ftx031","article-title":"Neisseria models of infection and persistence in the upper respiratory tract.","volume":"75","author":"Weyand","year":"2017","journal-title":"Pathog. Dis."},{"key":"B39","doi-asserted-by":"publisher","first-page":"717","DOI":"10.1016\/S1473-3099(18)30340-2","article-title":"Genetic characterisation of Neisseria gonorrhoeae resistant to both ceftriaxone and azithromycin.","volume":"18","author":"Whiley","year":"2018","journal-title":"Lancet Infect. Dis."},{"key":"B40","doi-asserted-by":"publisher","first-page":"8546","DOI":"10.1074\/jbc.R116.762906","article-title":"Natural product discovery from the human microbiome.","volume":"292","author":"Wilson","year":"2017","journal-title":"J. Biol. Chem."},{"key":"B41","year":"2012","journal-title":"Global Action Plan to Control the Spread and Impact of Antimicrobial Resistance in Neisseria gonorrhoeae."},{"key":"B42","doi-asserted-by":"publisher","first-page":"511","DOI":"10.1038\/nature18634","article-title":"Human commensals producing a novel antibiotic impair pathogen colonization.","volume":"535","author":"Zipperer","year":"2016","journal-title":"Nature"}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2020.577762\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,12,3]],"date-time":"2020-12-03T03:34:41Z","timestamp":1606966481000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2020.577762\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,12,3]]},"references-count":42,"alternative-id":["10.3389\/fmicb.2020.577762"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2020.577762","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,12,3]]},"article-number":"577762"}}