Abstract
Acinetobacter baumannii is a Gram-negative opportunistic zoonotic pathogenic bacterium that causes nosocomial infections ranging from minor to life-threatening. The clinical importance of this zoonotic pathogen is rapidly increasing due to the development of multiple resistance mechanisms and the synthesis of numerous virulence factors. Although no flagellum-mediated motility exists, it may move through twitching or surface-associated motility. Twitching motility is a coordinated multicellular movement caused by the extension, attachment, and retraction of type IV pili, which are involved in surface adherence and biofilm formation. Surface-associated motility is a kind of movement that does not need appendages and is most likely driven by the release of extra polymeric molecules. This kind of motility is linked to the production of 1,3-diaminopropane, lipooligosaccharide formation, natural competence, and efflux pump proteins. Since A. baumannii’s virulence qualities are directly tied to motility, it is possible that its motility may be used as a specialized preventative or therapeutic measure. The current review detailed the signaling mechanism and involvement of various proteins in controlling A. baumannii motility. As a result, we have thoroughly addressed the role of natural and synthetic compounds that impede A. baumannii motility, as well as the underlying action mechanisms. Understanding the regulatory mechanisms behind A. baumannii’s motility features will aid in the development of therapeutic drugs to control its infection.
Key points
• Acinetobacter baumannii exhibits multiple resistance mechanisms.
• A. baumannii can move owing to twitching and surface-associated motility.
• Natural and synthetic compounds can attenuate A. baumannii motility.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and materials
Not applicable.
References
Abdi SN, Ghotaslou R, Ganbarov K, Mobed A, Tanomand A, Yousefi M, Asgharzadeh M, Kafil HS (2020) Acinetobacter baumannii efflux pumps and antibiotic resistance. Infect Drug Resist 423–434. https://doi.org/10.2147/IDR.S228089
Abirami G, Durgadevi R, Velmurugan P, Ravi AV (2021) Gene expressing analysis indicates the role of pyrogallol as a novel antibiofilm and antivirulence agent against Acinetobacter baumannii. Arch Microbiol 203:251–260. https://doi.org/10.1007/s00203-020-02026-3
Ahmad I, Nygren E, Khalid F, Myint SL, Uhlin BE (2020) A cyclic-di-GMP signalling network regulates biofilm formation and surface associated motility of Acinetobacter baumannii 17978. Sci Rep 10(1):1991. https://doi.org/10.1038/s41598-020-58522-5
Al-Shamiri MM, Wang J, Zhang S, Li P, Odhiambo WO, Chen Y, Han B, Yang E, Xun M, Han L (2023) Probiotic Lactobacillus species and their biosurfactants eliminate Acinetobacter baumannii biofilm in various manners. Microbiol Spectr 11(2):e04614-e4622. https://doi.org/10.1128/spectrum.04614-22
Al-Shamiri MM, Zhang S, Mi P, Liu Y, Xun M, Yang E, Ai L, Han L, Chen Y (2021) Phenotypic and genotypic characteristics of Acinetobacter baumannii enrolled in the relationship among antibiotic resistance, biofilm formation and motility. Microb Pathog 155:104922. https://doi.org/10.1016/j.micpath.2021.104922
Armalytė J, Čepauskas A, Šakalytė G, Martinkus J, Skerniškytė J, Martens C, Sužiedėlienė E, Garcia-Pino A, Jurėnas D (2023) A polyamine acetyltransferase regulates the motility and biofilm formation of Acinetobacter baumannii. Nat Commun 14(1):3531. https://doi.org/10.1038/s41467-023-39316-5
Bamunuarachchi NI, Khan F, Kim Y-M (2021) Inhibition of virulence factors and biofilm formation of Acinetobacter baumannii by naturally-derived and synthetic drugs. Curr Drug Target 22(7):734–759. https://doi.org/10.2174/1389450121666201023122355
Barker J, Maxted H (1975) Observations on the growth and movement of Acinetobacter on semi-solid media. J Med Microbiol 8(3):443–446. https://doi.org/10.1099/00222615-8-3-443
Baumann P, Doudoroff M, Stanier R (1968) A study of the Moraxella group II. Oxidative-negative species (genus Acinetobacter). J Bacteriol 95(5):1520–1541. https://doi.org/10.1128/jb.95.5.1520-1541.1968
Blaschke U, Skiebe E, Wilharm G (2021) Novel genes required for surface-associated motility in Acinetobacter baumannii. Curr Microbiol 78:1509–1528. https://doi.org/10.1007/s00284-021-02407-x
Cerqueira GM, Kostoulias X, Khoo C, Aibinu I, Qu Y, Traven A, Peleg AY (2014) A global virulence regulator in Acinetobacter baumannii and its control of the phenylacetic acid catabolic pathway. J Infect Dis 210(1):46–55. https://doi.org/10.1093/infdis/jiu024
Chen R, Lv R, Xiao L, Wang M, Du Z, Tan Y, Cui Y, Yan Y, Luo Y, Yang R (2017) A1S_2811, a CheA/Y-like hybrid two-component regulator from Acinetobacter baumannii ATCC 17978, is involved in surface motility and biofilm formation in this bacterium. Microbiologyopen 6(5):e00510. https://doi.org/10.1002/mbo3.510
Clemmer KM, Bonomo RA, Rather PN (2011) Genetic analysis of surface motility in Acinetobacter baumannii. Microbiology 157(Pt 9):2534. https://doi.org/10.1099/mic.0.049791-0
Corral J, Pérez-Varela M, Barbé J, Aranda J (2020) Direct interaction between RecA and a CheW-like protein is required for surface-associated motility, chemotaxis and the full virulence of Acinetobacter baumannii strain ATCC 17978. Virulence 11(1):315–326. https://doi.org/10.1080/21505594.2020.1748923
Corral J, Pérez-Varela M, Sánchez-Osuna M, Cortés P, Barbé J, Aranda J (2021) Importance of twitching and surface-associated motility in the virulence of Acinetobacter baumannii. Virulence 12(1):2201–2213. https://doi.org/10.1080/21505594.2021.1950268
Craig L, Forest KT, Maier B (2019) Type IV pili: dynamics, biophysics and functional consequences. Nat Rev Microbiol 17(7):429–440. https://doi.org/10.1038/s41579-019-0195-4
de Dios R, Proctor CR, Maslova E, Dzalbe S, Rudolph CJ, McCarthy RR (2023) Artificial sweeteners inhibit multidrug-resistant pathogen growth and potentiate antibiotic activity. EMBO Mol Med 15(1):e16397. https://doi.org/10.15252/emmm.202216397
Dolzani L, Milan A, Scocchi M, Lagatolla C, Bressan R, Benincasa M (2019) Sub-MIC effects of a proline-rich antibacterial peptide on clinical isolates of Acinetobacter baumannii. J Med Microbiol 68(8):1253–1265. https://doi.org/10.1099/jmm.0.001028
Eijkelkamp BA, Hassan KA, Paulsen IT, Brown MH (2011a) Investigation of the human pathogen Acinetobacter baumannii under iron limiting conditions. BMC Genom 12:1–14. https://doi.org/10.1186/1471-2164-12-126
Eijkelkamp BA, Stroeher UH, Hassan KA, Papadimitrious MS, Paulsen IT, Brown MH, Lo R (2011b) Adherence and motility characteristics of clinical Acinetobacter baumannii isolates. FEMS Microbiol Lett 323(1):44–51. https://doi.org/10.1111/j.1574-6968.2011.02362.x
Elshaer SL, Shaldam MA, Shaaban MI (2022) Ketoprofen, piroxicam and indomethacin-suppressed quorum sensing and virulence factors in Acinetobacter baumannii. J Appl Microbiol 133(4):2182–2197. https://doi.org/10.1111/jam.15609
Gedefie A, Demsis W, Ashagrie M, Kassa Y, Tesfaye M, Tilahun M, Bisetegn H, Sahle Z (2021) Acinetobacter baumannii biofilm formation and its role in disease pathogenesis: a review. Infect Drug Resist 3711–3719. https://doi.org/10.2147/IDR.S332051
Harding CM, Hennon SW, Feldman MF (2018) Uncovering the mechanisms of Acinetobacter baumannii virulence. Nat Rev Microbiol 16(2):91–102. https://doi.org/10.1038/nrmicro.2017.148
Harding CM, Tracy EN, Carruthers MD, Rather PN, Actis LA, Munson Jr RS (2013) Acinetobacter baumannii strain M2 produces type IV pili which play a role in natural transformation and twitching motility but not surface-associated motility. MBio 4(4). https://doi.org/10.1128/mbio.00360-13
Henrichsen J (1972) Bacterial surface translocation: a survey and a classification. Bacteriol Rev 36(4):478–503. https://doi.org/10.1128/br.36.4.478-503.1972
Ibrahim S, Al-Saryi N, Al-Kadmy IM, Aziz SN (2021) Multidrug-resistant Acinetobacter baumannii as an emerging concern in hospitals. Mol Biol Rep 48(10):6987–6998. https://doi.org/10.1007/s11033-021-06690-6
Islam MM, Kim K, Lee JC, Shin M (2021) LeuO, a LysR-type transcriptional regulator, is involved in biofilm formation and virulence of Acinetobacter baumannii. Front Cell Infect Microbiol 11:738706. https://doi.org/10.3389/fcimb.2021.738706
Jothipandiyan S, Suresh D, Sankaran SV, Thamotharan S, Shanmugasundaram K, Vincent P, Sekaran S, Gowrishankar S, Pandian SK, Paramasivam N (2022) Heteroleptic pincer palladium (II) complex coated orthopedic implants impede the AbaI/AbaR quorum sensing system and biofilm development by Acinetobacter baumannii. Biofouling 38(1):55–70. https://doi.org/10.1080/08927014.2021.2015336
Kaushik V, Tiwari M, Joshi R, Tiwari V (2022) Therapeutic strategies against potential antibiofilm targets of multidrug-resistant Acinetobacter baumannii. J Cell Physiol 237(4):2045–2063. https://doi.org/10.1002/jcp.30683
Kearns DB (2010) A field guide to bacterial swarming motility. Nat Rev Microbiol 8(9):634–644. https://doi.org/10.1038/nrmicro2405
Khadke SK, Lee J-H, Kim Y-G, Raj V, Lee J (2021) Assessment of antibiofilm potencies of nervonic and oleic acid against Acinetobacter baumannii using in vitro and computational approaches. Biomedicines 9(9):1133. https://doi.org/10.3390/biomedicines9091133
Khadke SK, Lee J-H, Woo J-T, Lee J (2019) Inhibitory effects of honokiol and magnolol on biofilm formation by Acinetobacter baumannii. Biotechnol Bioprocess Eng 24:359–365. https://doi.org/10.1007/s12257-019-0006-9
Khan F, Pham DT, Oloketuyi SF, Kim Y-M (2020a) Antibiotics application strategies to control biofilm formation in pathogenic bacteria. Curr Pharm Biotechnol 21(4):270–286. https://doi.org/10.2174/1389201020666191112155905
Khan F, Pham DTN, Oloketuyi SF, Kim Y-M (2020b) Regulation and controlling the motility properties of Pseudomonas aeruginosa. Appl Microbiol Biotechnol 104:33–49. https://doi.org/10.1007/s00253-019-10201-w
Kim H-J, Kim N-Y, Ko S-Y, Park S-Y, Oh M-H, Shin M-S, Lee Y-C, Lee J-C (2022) Complementary regulation of BfmRS two-component and AbaIR quorum sensing systems to express virulence-associated genes in Acinetobacter baumannii. Int J Mol Sci 23(21):13136. https://doi.org/10.3390/ijms232113136
Kim H-R, Shin D-S, Jang H-I, Eom Y-B (2020) Anti-biofilm and anti-virulence effects of zerumbone against Acinetobacter baumannii. Microbiology 166(8):717–726. https://doi.org/10.1099/mic.0.000930
Kim N, Son JH, Kim K, Kim HJ, Kim YJ, Shin M, Lee JC (2021) Global regulator DksA modulates virulence of Acinetobacter baumannii. Virulence 12(1):2750–2763. https://doi.org/10.1080/21505594.2021.1995253
Li H, Du X, Chen C, Qi J, Wang Y (2022) Integrating transcriptomics and metabolomics analysis on kojic acid combating Acinetobacter baumannii biofilm and its potential roles. Microbiol Res 254:126911. https://doi.org/10.1016/j.micres.2021.126911
Lin H, Zhou C, Yu K-H, Lin Y-S, Wang L-B, Zhang Y, Liu S-X, Xu W-Y, Sun Y, Zhou T-L (2023) Glabridin functions as a quorum sensing inhibitor to inhibit biofilm formation and swarming motility of multidrug-resistant Acinetobacter baumannii. Infect Drug Resist 5697–5705. https://doi.org/10.2147/IDR.S417751
Liu W, Wu Z, Mao C, Guo G, Zeng Z, Fei Y, Wan S, Peng J, Wu J (2020) Antimicrobial peptide Cec4 eradicates the bacteria of clinical carbapenem-resistant Acinetobacter baumannii biofilm. Front Microbiol 11:1532. https://doi.org/10.3389/fmicb.2020.01532
López-Martín M, Dubern J-F, Alexander MR, Williams P (2021) AbaM regulates quorum sensing, biofilm formation, and virulence in Acinetobacter baumannii. J Bacteriol 203(8). https://doi.org/10.1128/jb.00635-20
Mattick JS (2002) Type IV pili and twitching motility. Annu Rev Microbiol 56(1):289–314. https://doi.org/10.1146/annurev.micro.56.012302.160938
McQueary CN, Kirkup BC, Si Y, Barlow M, Actis LA, Craft DW, Zurawski DV (2012) Extracellular stress and lipopolysaccharide modulate Acinetobacter baumannii surface-associated motility. J Microbiol 50:434–443. https://doi.org/10.1007/s12275-012-1555-1
Mea HJ, Yong PVC, Wong EH (2021) An overview of Acinetobacter baumannii pathogenesis: motility, adherence and biofilm formation. Microbiol Res 247:126722. https://doi.org/10.1016/j.micres.2021.126722
Mickymaray S (2019) Efficacy and mechanism of traditional medicinal plants and bioactive compounds against clinically important pathogens. Antibiotics 8(4):257. https://doi.org/10.3390/antibiotics8040257
Mussi MA, Gaddy JA, Cabruja M, Arivett BA, Viale AM, Rasia R, Actis LA (2010) The opportunistic human pathogen Acinetobacter baumannii senses and responds to light. J Bacteriol 192(24):6336–6345. https://doi.org/10.1128/jb.00917-10
Oh MH, Han K (2020) AbaR is a LuxR type regulator essential for motility and the formation of biofilm and pellicle in Acinetobacter baumannii. Genes Genom 42:1339–1346. https://doi.org/10.1007/s13258-020-01005-8
Oloketuyi SF, Khan F (2017) Strategies for biofilm inhibition and virulence attenuation of foodborne pathogen-Escherichia coli O157: H7. Curr Microbiol 74:1477–1489. https://doi.org/10.1007/s00284-017-1314-y
Organization WH (2017) Antibacterial agents in clinical development: an analysis of the antibacterial clinical development pipeline, including tuberculosis. World Health Organization
Ottemann KM, Miller JF (1997) Roles for motility in bacterial–host interactions. Mol Microbiol 24(6):1109–1117. https://doi.org/10.1046/j.1365-2958.1997.4281787.x
Pérez-Varela M, Corral J, Aranda J, Barbé J (2019) Roles of efflux pumps from different superfamilies in the surface-associated motility and virulence of Acinetobacter baumannii ATCC 17978. Antimicrob Agents Chemother 63(3). https://doi.org/10.1128/aac.45.12.3293-3303.2001
Pérez-Varela M, Corral J, Vallejo JA, Rumbo-Feal S, Bou G, Aranda J, Barbé J (2017) Mutations in the β-Subunit of the RNA polymerase impair the surface-associated motility and virulence of Acinetobacter baumannii. Infect Immun 85(8). https://doi.org/10.1128/iai.00327-17
Rajkumari J, Siddhardha B (2020) Acinetobacter baumannii: infections and drug resistance. Model Organisms for Microbial Pathogenesis, Biofilm Formation and Antimicrobial Drug Discovery 257–271. https://doi.org/10.1007/978-981-15-1695-5_11
Raorane CJ, Lee J-H, Kim Y-G, Rajasekharan SK, García-Contreras R, Lee J (2019) Antibiofilm and antivirulence efficacies of flavonoids and curcumin against Acinetobacter baumannii. Front Microbiol 10:990. https://doi.org/10.3389/fmicb.2019.00990
Raorane CJ, Lee J-H, Lee J (2020) Rapid killing and biofilm inhibition of multidrug-resistant Acinetobacter baumannii strains and other microbes by iodoindoles. Biomolecules 10(8):1186. https://doi.org/10.3390/biom10081186
Rasamiravaka T, Labtani Q, Duez P, El Jaziri M (2015) The formation of biofilms by Pseudomonas aeruginosa: a review of the natural and synthetic compounds interfering with control mechanisms. Biomed Res Int 2015. https://doi.org/10.1155/2015/759348
Roy S, Chowdhury G, Mukhopadhyay AK, Dutta S, Basu S (2022) Convergence of biofilm formation and antibiotic resistance in Acinetobacter baumannii infection. Front Med 9:793615. https://doi.org/10.3389/fmed.2022.793615
Seleem NM, Abd El Latif HK, Shaldam MA, El-Ganiny A (2020) Drugs with new lease of life as quorum sensing inhibitors: for combating MDR Acinetobacter baumannii infections. Eur J Clin Microbiol Infect Dis 39:1687–1702. https://doi.org/10.1007/s10096-020-03882-z
Selvaraj A, Valliammai A, Sivasankar C, Suba M, Sakthivel G, Pandian SK (2020) Antibiofilm and antivirulence efficacy of myrtenol enhances the antibiotic susceptibility of Acinetobacter baumannii. Sci Rep 10(1):21975. https://doi.org/10.1038/s41598-020-79128-x
Shin D-S, Eom Y-B (2020) Antimicrobial and antibiofilm activities of Clostridium butyricum supernatant against Acinetobacter baumannii. Arch Microbiol 202(5):1059–1068. https://doi.org/10.1007/s00203-020-01823-0
Skiebe E, de Berardinis V, Morczinek P, Kerrinnes T, Faber F, Lepka D, Hammer B, Zimmermann O, Ziesing S, Wichelhaus TA (2012) Surface-associated motility, a common trait of clinical isolates of Acinetobacter baumannii, depends on 1, 3-diaminopropane. Int J Med Microbiol 302(3):117–128. https://doi.org/10.1016/j.ijmm.2012.03.003
Tapia-Rodriguez MR, Cantu-Soto EU, Vazquez-Armenta FJ, Bernal-Mercado AT, Ayala-Zavala JF (2023) Inhibition of Acinetobacter baumannii biofilm formation by terpenes from oregano (Lippia graveolens) essential oil. Antibiotics 12(10):1539. https://doi.org/10.3390/antibiotics12101539
Tipton KA, Rather PN (2017) An ompR-envZ two-component system ortholog regulates phase variation, osmotic tolerance, motility, and virulence in Acinetobacter baumannii strain AB5075. J Bacteriol 199(3). https://doi.org/10.1128/jb.00705-16
Ušjak D, Dinić M, Novović K, Ivković B, Filipović N, Stevanović M, Milenković MT (2021) Methoxy-substituted hydroxychalcone reduces biofilm production, adhesion and surface motility of Acinetobacter baumannii by inhibiting ompA gene expression. Chem Biodivers 18(1):e2000786. https://doi.org/10.1002/cbdv.202000786
Ušjak D, Ivković B, Božić DD, Bošković L, Milenković M (2019) Antimicrobial activity of novel chalcones and modulation of virulence factors in hospital strains of Acinetobacter baumannii and Pseudomonas aeruginosa. Microb Pathog 131:186–196. https://doi.org/10.1016/j.micpath.2019.04.015
Vesel N, Blokesch M (2021) Pilus production in Acinetobacter baumannii is growth phase dependent and essential for natural transformation. J Bacteriol 203(8). https://doi.org/10.1128/jb.00034-21
Vijayakumar S, Rajenderan S, Laishram S, Anandan S, Balaji V, Biswas I (2016) Biofilm formation and motility depend on the nature of the Acinetobacter baumannii clinical isolates. Front Public Health 4:105. https://doi.org/10.3389/fpubh.2016.00105
Vo N, Sidner BS, Yu Y, Piepenbrink KH (2023) Type IV pilus-mediated inhibition of Acinetobacter baumannii biofilm formation by phenothiazine compounds. Microbiol Spectr e01023–23. https://doi.org/10.1128/spectrum.01023-23
Weinberg S, Villedieu A, Bagdasarian N, Karah N, Teare L, Elamin W (2020) Control and management of multidrug resistant Acinetobacter baumannii: a review of the evidence and proposal of novel approaches. Infect Prev Pract 2(3):100077. https://doi.org/10.1016/j.infpip.2020.100077
Whiteway C, Breine A, Philippe C, Van der Henst C (2022) Acinetobacter baumannii. Trends Microbiol 30(2):199–200. https://doi.org/10.1016/j.tim.2021.11.008
Wilharm G, Piesker J, Laue M, Skiebe E (2013) DNA uptake by the nosocomial pathogen Acinetobacter baumannii occurs during movement along wet surfaces. J Bacteriol 195(18):4146–4153. https://doi.org/10.1128/JB.00754-13
Wood CR, Ohneck EJ, Edelmann RE, Actis LA (2018) A light-regulated type I pilus contributes to Acinetobacter baumannii biofilm, motility, and virulence functions. Infect Immun 86(9). https://doi.org/10.1128/iai.00442-18
Funding
This research was supported by the Basic Science Research Program through the National Research Foundation (NRF) of Korea grant funded by the Ministry of Education (2021R1A6A1A03039211 and 2022R1A2B5B01001998). This research was also supported by Basic Science Research Program through the NRF of Korea, funded by the Ministry of Education (RS-2023–00241461 to F. Khan).
Author information
Authors and Affiliations
Contributions
Geum-Jae Jeong: literature search, writing-original draft and editing. Fazlurrahman Khan: conceptualization, funding, supervising, literature search, writing-review and editing. Nazia Tabassum: writing and editing. Young-Mog Kim: supervision, funding, writing-review and editing.
Corresponding authors
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Jeong, GJ., Khan, F., Tabassum, N. et al. Motility of Acinetobacter baumannii: regulatory systems and controlling strategies. Appl Microbiol Biotechnol 108, 3 (2024). https://doi.org/10.1007/s00253-023-12975-6
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00253-023-12975-6