{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T17:51:10Z","timestamp":1788285070962,"version":"build-2803163510"},"reference-count":39,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2026,3,27]],"date-time":"2026-03-27T00:00:00Z","timestamp":1774569600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0"},{"start":{"date-parts":[[2026,5,6]],"date-time":"2026-05-06T00:00:00Z","timestamp":1778025600000},"content-version":"vor","delay-in-days":40,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32370105 and 32570139"],"award-info":[{"award-number":["32370105 and 32570139"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Microbiol"],"DOI":"10.1186\/s12866-026-05003-w","type":"journal-article","created":{"date-parts":[[2026,3,26]],"date-time":"2026-03-26T23:33:07Z","timestamp":1774567987000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Retrieving of diguanylate cyclases responsible for biofilm formation and antibiotic resistance in Acinetobacter baumannii"],"prefix":"10.1186","volume":"26","author":[{"given":"Boqiao","family":"Li","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ling","family":"Zou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1865-4403","authenticated-orcid":false,"given":"Xiaobo","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2026,3,27]]},"reference":[{"issue":"8","key":"5003_CR1","doi-asserted-by":"publisher","first-page":"1079","DOI":"10.1086\/533452","volume":"197","author":"LB Rice","year":"2008","unstructured":"Rice LB. Federal funding for the study of antimicrobial resistance in nosocomial pathogens: no ESKAPE. J Infect Dis. 2008;197(8):1079\u201381.","journal-title":"J Infect Dis"},{"key":"5003_CR2","doi-asserted-by":"publisher","first-page":"441","DOI":"10.3389\/fimmu.2017.00441","volume":"8","author":"MG Garc\u00eda-Pati\u00f1o","year":"2017","unstructured":"Garc\u00eda-Pati\u00f1o MG, Garc\u00eda-Contreras R, Licona-Lim\u00f3n P. The immune response against Acinetobacter baumannii, an emerging pathogen in nosocomial infections. Front Immunol. 2017;8:441.","journal-title":"Front Immunol."},{"key":"5003_CR3","doi-asserted-by":"publisher","first-page":"512","DOI":"10.3389\/fmicb.2014.00512","volume":"5","author":"V Tiwari","year":"2014","unstructured":"Tiwari V, Tiwari M. Quantitative proteomics to study carbapenem resistance in Acinetobacter baumannii. Front Microbiol. 2014;5:512.","journal-title":"Front Microbiol."},{"key":"5003_CR4","doi-asserted-by":"publisher","first-page":"55","DOI":"10.3389\/fcimb.2017.00055","volume":"7","author":"C-R Lee","year":"2017","unstructured":"Lee C-R, Lee JH, Park M, Park KS, Bae IK, Kim YB, Cha C-J, Jeong BC, Lee SH. Biology of Acinetobacter baumannii: pathogenesis, antibiotic resistance mechanisms, and prospective treatment options. Front Cell Infect Microbiol. 2017;7:55.","journal-title":"Front Cell Infect Microbiol."},{"issue":"1","key":"5003_CR5","doi-asserted-by":"publisher","first-page":"12","DOI":"10.3390\/genes8010012","volume":"8","author":"C Kr\u00f6ger","year":"2017","unstructured":"Kr\u00f6ger C, Kary SC, Schauer K, Cameron ADS. Genetic regulation of virulence and antibiotic resistance in Acinetobacter baumannii. Genes. 2017;8(1):12.","journal-title":"Genes"},{"issue":"1","key":"5003_CR6","doi-asserted-by":"publisher","first-page":"22068","DOI":"10.1038\/s41598-024-73258-2","volume":"14","author":"H-L Zhang","year":"2024","unstructured":"Zhang H-L, Nizamani MM, Wang Y, Cui X, Xiu H, Qayyum M, et al. Analysis of antimicrobial resistance and genetic diversity of Acinetobacter baumannii in a tertiary care hospital in Haikou City. Sci Rep. 2024;14(1):22068.","journal-title":"Sci Rep"},{"issue":"8","key":"5003_CR7","doi-asserted-by":"publisher","first-page":"1854","DOI":"10.1038\/s41564-025-02059-8","volume":"10","author":"NM Quijada","year":"2025","unstructured":"Quijada NM, Cobo-D\u00edaz JF, Valentino V, Barcenilla C, De Filippis F, Cabrera-Rubio R, et al. The food-associated resistome is shaped by processing and production environments. Nat Microbiol. 2025;10(8):1854\u201367.","journal-title":"Nat Microbiol"},{"key":"5003_CR8","doi-asserted-by":"publisher","first-page":"122","DOI":"10.1016\/j.micpath.2017.04.039","volume":"108","author":"AM Bardbari","year":"2017","unstructured":"Bardbari AM, Arabestani MR, Karami M, Keramat F, Alikhani MY, Bagheri KP. Correlation between ability of biofilm formation with their responsible genes and MDR patterns in clinical and environmental Acinetobacter baumannii isolates. Microb Pathog. 2017;108:122\u20138.","journal-title":"Microb Pathog"},{"issue":"3","key":"5003_CR9","doi-asserted-by":"publisher","first-page":"29","DOI":"10.3390\/microorganisms4030029","volume":"4","author":"GJ Da Silva","year":"2016","unstructured":"Da Silva GJ, Domingues S. Insights on the horizontal gene transfer of carbapenemase determinants in the opportunistic pathogen Acinetobacter baumannii. Microorganisms. 2016;4(3):29.","journal-title":"Microorganisms"},{"issue":"2","key":"5003_CR10","doi-asserted-by":"publisher","first-page":"243","DOI":"10.1007\/s12275-011-0343-7","volume":"49","author":"CN McQueary","year":"2011","unstructured":"McQueary CN, Actis LA. Acinetobacter baumannii biofilms: variations among strains and correlations with other cell properties. J Microbiol. 2011;49(2):243\u201350.","journal-title":"J Microbiol"},{"issue":"3","key":"5003_CR11","doi-asserted-by":"publisher","first-page":"434","DOI":"10.1007\/s12275-012-1555-1","volume":"50","author":"CN McQueary","year":"2012","unstructured":"McQueary CN, Kirkup BC, Si Y, Barlow M, Actis LA, Craft DW, et al. Extracellular stress and lipopolysaccharide modulate Acinetobacter baumannii surface-associated motility. J Microbiol. 2012;50(3):434\u201343.","journal-title":"J Microbiol"},{"issue":"4","key":"5003_CR12","doi-asserted-by":"publisher","first-page":"e00360","DOI":"10.1128\/mbio.00360-00313","volume":"4","author":"CM Harding","year":"2013","unstructured":"Harding CM, Tracy EN, Carruthers MD, Rather PN, Actis LA, Munson RS. Acinetobacter baumannii strain M2 produces type IV pili which play a role in natural transformation and twitching motility but not surface-associated motility. MBio. 2013;4(4):e00360-e413. https:\/\/doi.org\/10.1128\/mbio.00360-00313.","journal-title":"MBio"},{"issue":"6101","key":"5003_CR13","doi-asserted-by":"publisher","first-page":"279","DOI":"10.1038\/325279a0","volume":"325","author":"P Ross","year":"1987","unstructured":"Ross P, Weinhouse H, Aloni Y, Michaeli D, Weinberger-Ohana P, Mayer R, et al. Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature. 1987;325(6101):279\u201381.","journal-title":"Nature"},{"key":"5003_CR14","doi-asserted-by":"crossref","unstructured":"R\u00f6mling U, Galperin MY: Discovery of the second messenger cyclic di-GMP. In: c-di-GMP Signaling: Methods and Protocols. Edited by Sauer K. New York, NY: Springer New York; 2017: 1\u20138.","DOI":"10.1007\/978-1-4939-7240-1_1"},{"issue":"1","key":"5003_CR15","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1128\/MMBR.00043-12","volume":"77","author":"U R\u00f6mling","year":"2013","unstructured":"R\u00f6mling U, Galperin MY, Gomelsky M. Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev. 2013;77(1):1\u201352.","journal-title":"Microbiol Mol Biol Rev"},{"issue":"5","key":"5003_CR16","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1038\/nrmicro.2016.190","volume":"15","author":"U Jenal","year":"2017","unstructured":"Jenal U, Reinders A, Lori C. Cyclic di-GMP: second messenger extraordinaire. Nat Rev Microbiol. 2017;15(5):271\u201384.","journal-title":"Nat Rev Microbiol"},{"issue":"9","key":"5003_CR17","doi-asserted-by":"publisher","first-page":"1378","DOI":"10.1016\/j.intimp.2011.03.024","volume":"11","author":"L Zhao","year":"2011","unstructured":"Zhao L, KuoLee R, Harris G, Tram K, Yan H, Chen W. C-di-GMP protects against intranasal Acinetobacter baumannii infection in mice by chemokine induction and enhanced neutrophil recruitment. Int Immunopharmacol. 2011;11(9):1378\u201383.","journal-title":"Int Immunopharmacol"},{"issue":"19","key":"5003_CR18","doi-asserted-by":"publisher","first-page":"3683","DOI":"10.1016\/j.jmb.2016.07.023","volume":"428","author":"T Schirmer","year":"2016","unstructured":"Schirmer T. C-di-GMP synthesis: structural aspects of evolution, catalysis and regulation. J Mol Biol. 2016;428(19):3683\u2013701.","journal-title":"J Mol Biol"},{"issue":"18","key":"5003_CR19","doi-asserted-by":"publisher","first-page":"5970","DOI":"10.1093\/nar\/gkq382","volume":"38","author":"ASN Seshasayee","year":"2010","unstructured":"Seshasayee ASN, Fraser GM, Luscombe NM. Comparative genomics of cyclic-di-GMP signalling in bacteria: post-translational regulation and catalytic activity. Nucleic Acids Res. 2010;38(18):5970\u201381.","journal-title":"Nucleic Acids Res"},{"key":"5003_CR20","doi-asserted-by":"publisher","first-page":"107915","DOI":"10.1016\/j.biotechadv.2022.107915","volume":"56","author":"X Liu","year":"2022","unstructured":"Liu X, Cao B, Yang L, Gu J-D. Biofilm control by interfering with c-di-GMP metabolism and signaling. Biotechnol Adv. 2022;56:107915.","journal-title":"Biotechnol Adv"},{"issue":"10","key":"5003_CR21","doi-asserted-by":"publisher","first-page":"724","DOI":"10.1038\/nrmicro2203","volume":"7","author":"T Schirmer","year":"2009","unstructured":"Schirmer T, Jenal U. Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol. 2009;7(10):724\u201335.","journal-title":"Nat Rev Microbiol"},{"issue":"15","key":"5003_CR22","doi-asserted-by":"publisher","first-page":"4722","DOI":"10.1128\/JB.00327-09","volume":"191","author":"F Rao","year":"2009","unstructured":"Rao F, Qi Y, Chong HS, Kotaka M, Li B, Li J, et al. The functional role of a conserved loop in EAL domain-based cyclic di-GMP-specific phosphodiesterase. J Bacteriol. 2009;191(15):4722\u201331.","journal-title":"J Bacteriol"},{"issue":"7249","key":"5003_CR23","doi-asserted-by":"publisher","first-page":"1015","DOI":"10.1038\/nature07966","volume":"459","author":"TRM Barends","year":"2009","unstructured":"Barends TRM, Hartmann E, Griese JJ, Beitlich T, Kirienko NV, Ryjenkov DA, et al. Structure and mechanism of a bacterial light-regulated cyclic nucleotide phosphodiesterase. Nature. 2009;459(7249):1015\u20138.","journal-title":"Nature"},{"key":"5003_CR24","doi-asserted-by":"publisher","first-page":"261","DOI":"10.1146\/annurev-micro-121809-151631","volume":"65","author":"JT Henry","year":"2011","unstructured":"Henry JT, Crosson S. Ligand-binding PAS domains in a genomic, cellular, and structural context. Annual Review of Microbiology. 2011;65:261\u201386.","journal-title":"Annual Review of Microbiology"},{"issue":"5","key":"5003_CR25","doi-asserted-by":"publisher","first-page":"e00790","DOI":"10.1128\/jb.00790-00716","volume":"199","author":"U R\u00f6mling","year":"2017","unstructured":"R\u00f6mling U, Liang Z-X, Dow JM. Progress in understanding the molecular basis underlying functional diversification of cyclic dinucleotide turnover proteins. J Bacteriol. 2017;199(5):e00790-e816. https:\/\/doi.org\/10.1128\/jb.00790-00716.","journal-title":"J Bacteriol"},{"issue":"1","key":"5003_CR26","doi-asserted-by":"publisher","first-page":"1991","DOI":"10.1038\/s41598-020-58522-5","volume":"10","author":"I Ahmad","year":"2020","unstructured":"Ahmad I, Nygren E, Khalid F, Myint SL, Uhlin BE. A cyclic-di-GMP signalling network regulates biofilm formation and surface associated motility of Acinetobacter baumannii 17978. Sci Rep. 2020;10(1):1991.","journal-title":"Sci Rep"},{"issue":"11","key":"5003_CR27","doi-asserted-by":"publisher","first-page":"1406","DOI":"10.1038\/s41589-024-01740-z","volume":"20","author":"X Liu","year":"2024","unstructured":"Liu X, Zou L, Li B, Di Martino P, Rittschof D, Yang J-L, et al. Chemical signaling in biofilm-mediated biofouling. Nat Chem Biol. 2024;20(11):1406\u201319.","journal-title":"Nat Chem Biol"},{"issue":"1","key":"5003_CR28","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1038\/s41522-023-00465-6","volume":"9","author":"I Ahmad","year":"2023","unstructured":"Ahmad I, Nadeem A, Mushtaq F, Zlatkov N, Shahzad M, Zavialov AV, et al. Csu pili dependent biofilm formation and virulence of Acinetobacter baumannii. NPJ Biofilms Microbiomes. 2023;9(1):101.","journal-title":"NPJ Biofilms Microbiomes"},{"issue":"4","key":"5003_CR29","doi-asserted-by":"publisher","first-page":"e01313","DOI":"10.1128\/mbio.01313-01314","volume":"5","author":"AT Tucker","year":"2014","unstructured":"Tucker AT, Nowicki EM, Boll JM, Knauf GA, Burdis NC, Trent MS, et al. Defining gene-phenotype relationships in Acinetobacter baumannii through one-step chromosomal gene inactivation. MBio. 2014;5(4):e01313-e1314. https:\/\/doi.org\/10.1128\/mbio.01313-01314.","journal-title":"MBio"},{"issue":"21","key":"5003_CR30","doi-asserted-by":"publisher","first-page":"5558","DOI":"10.1073\/pnas.1800961115","volume":"115","author":"N Pakharukova","year":"2018","unstructured":"Pakharukova N, Tuittila M, Paavilainen S, Malmi H, Parilova O, Teneberg S, et al. Structural basis for Acinetobacter baumannii biofilm formation. Proc Natl Acad Sci U S A. 2018;115(21):5558\u201363.","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"35","key":"5003_CR31","doi-asserted-by":"publisher","first-page":"e2516964122","DOI":"10.1073\/pnas.2516964122","volume":"122","author":"D Sun","year":"2025","unstructured":"Sun D, Liu X, Zhang Y, Shi R, Ru Y, Zhou X, et al. Local c-di-GMP signaling, triggered by cross-regulation of cAMP-CRP and c-di-GMP, controls biofilm formation under nutrient limitation. Proc Natl Acad Sci U S A. 2025;122(35):e2516964122.","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"15","key":"5003_CR32","doi-asserted-by":"publisher","first-page":"5178","DOI":"10.1128\/JB.00375-08","volume":"190","author":"LM Holland","year":"2008","unstructured":"Holland LM, O\u2019Donnell ST, Ryjenkov DA, Gomelsky L, Slater SR, Fey PD, et al. A staphylococcal GGDEF domain protein regulates biofilm formation independently of cyclic dimeric GMP. J Bacteriol. 2008;190(15):5178\u201389.","journal-title":"J Bacteriol"},{"issue":"6","key":"5003_CR33","doi-asserted-by":"publisher","first-page":"1216","DOI":"10.1111\/mmi.12428","volume":"90","author":"I Ahmad","year":"2013","unstructured":"Ahmad I, Wigren E, Le Guyon S, Vekkeli S, Blanka A, el Mouali Y, et al. The EAL-like protein STM1697 regulates virulence phenotypes, motility and biofilm formation in Salmonella typhimurium. Mol Microbiol. 2013;90(6):1216\u201332.","journal-title":"Mol Microbiol"},{"issue":"1","key":"5003_CR34","doi-asserted-by":"publisher","first-page":"143","DOI":"10.1038\/s41522-024-00619-0","volume":"10","author":"M Siri","year":"2024","unstructured":"Siri M, V\u00e1zquez-D\u00e1vila M, Sotelo Guzman C, Bidan CM. Nutrient availability influences E. coli biofilm properties and the structure of purified curli amyloid fibers. NPJ Biofilms Microbiomes. 2024;10(1):143.","journal-title":"NPJ Biofilms Microbiomes"},{"issue":"11","key":"5003_CR35","doi-asserted-by":"publisher","first-page":"1234","DOI":"10.1007\/s00018-005-4557-x","volume":"62","author":"U R\u00f6mling","year":"2005","unstructured":"R\u00f6mling U. Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell Mol Life Sci CMLS. 2005;62(11):1234\u201346.","journal-title":"Cell Mol Life Sci CMLS"},{"issue":"9","key":"5003_CR36","doi-asserted-by":"publisher","first-page":"563","DOI":"10.1038\/nrmicro.2016.94","volume":"14","author":"H-C Flemming","year":"2016","unstructured":"Flemming H-C, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S. Biofilms: an emergent form of bacterial life. Nat Rev Microbiol. 2016;14(9):563\u201375.","journal-title":"Nat Rev Microbiol"},{"issue":"10","key":"5003_CR37","doi-asserted-by":"publisher","first-page":"e01049","DOI":"10.1128\/AAC.01049-18","volume":"62","author":"B Poudyal","year":"2018","unstructured":"Poudyal B, Sauer K. The PA3177 gene encodes an active diguanylate cyclase that contributes to biofilm antimicrobial tolerance but not biofilm formation by Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2018;62(10):e01049-e1118.","journal-title":"Antimicrob Agents Chemother"},{"issue":"3","key":"5003_CR38","doi-asserted-by":"publisher","first-page":"488","DOI":"10.1111\/mmi.12587","volume":"92","author":"K Gupta","year":"2014","unstructured":"Gupta K, Liao J, Petrova OE, Cherny KE, Sauer K. Elevated levels of the second messenger c-di-GMP contribute to antimicrobial resistance of Pseudomonas aeruginosa. Mol Microbiol. 2014;92(3):488\u2013506.","journal-title":"Mol Microbiol"},{"issue":"6","key":"5003_CR39","doi-asserted-by":"publisher","first-page":"2316","DOI":"10.1021\/acssynbio.5c00193","volume":"14","author":"Y Hu","year":"2025","unstructured":"Hu Y, Liu J, Teng A, Zhang Y, Yang L, Cao B. Sensitive and broadly compatible transcription factor-based biosensor for monitoring c-di-GMP dynamics in biofilms. ACS Synth Biol. 2025;14(6):2316\u201327.","journal-title":"ACS Synth Biol"}],"container-title":["BMC Microbiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12866-026-05003-w","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12866-026-05003-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12866-026-05003-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,5,5]],"date-time":"2026-05-05T23:16:16Z","timestamp":1778022976000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1186\/s12866-026-05003-w"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,3,27]]},"references-count":39,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2026,12]]}},"alternative-id":["5003"],"URL":"https:\/\/doi.org\/10.1186\/s12866-026-05003-w","relation":{},"ISSN":["1471-2180"],"issn-type":[{"value":"1471-2180","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,3,27]]},"assertion":[{"value":"6 February 2026","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 March 2026","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"27 March 2026","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"437"}}