Rheotaxis in Mycoplasma gliding.
Mycoplasma pneumoniae
cell shape
fluid flow
gliding motility
optical microscopy
signal transduction
Journal
Microbiology and immunology
ISSN: 1348-0421
Titre abrégé: Microbiol Immunol
Pays: Australia
ID NLM: 7703966
Informations de publication
Date de publication:
Sep 2023
Sep 2023
Historique:
revised:
22
06
2023
received:
01
06
2023
accepted:
23
06
2023
medline:
5
9
2023
pubmed:
11
7
2023
entrez:
10
7
2023
Statut:
ppublish
Résumé
This review describes the upstream-directed movement in the small parasitic bacterium Mycoplasma. Many Mycoplasma species exhibit gliding motility, a form of biological motion over surfaces without the aid of general surface appendages such as flagella. The gliding motility is characterized by a constant unidirectional movement without changes in direction or backward motion. Unlike flagellated bacteria, Mycoplasma lacks the general chemotactic signaling system to control their moving direction. Therefore, the physiological role of directionless travel in Mycoplasma gliding remains unclear. Recently, high-precision measurements under an optical microscope have revealed that three species of Mycoplasma exhibited rheotaxis, that is, the direction of gliding motility is lead upstream by the water flow. This intriguing response appears to be optimized for the flow patterns encountered at host surfaces. This review provides a comprehensive overview of the morphology, behavior, and habitat of Mycoplasma gliding, and discusses the possibility that the rheotaxis is ubiquitous among them.
Identifiants
pubmed: 37430383
doi: 10.1111/1348-0421.13090
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
389-395Subventions
Organisme : Naito Foundation
Organisme : Kato Memorial Bioscience Foundation
Organisme : Japan Society for the Promotion of Science
ID : 22H05066
Organisme : Japan Society for the Promotion of Science
ID : 21K07020
Organisme : Japan Society for the Promotion of Science
ID : 20H05543
Informations de copyright
© 2023 The Societies and John Wiley & Sons Australia, Ltd.
Références
Rosengarten R, Klein-Struckmeier A, Kirchhoff H. Rheotactic behavior of a gliding mycoplasma. J Bacteriol. 1988;170:989-990. https://doi.org/10.1128/jb.170.2.989-990.1988
Coombs S, Bak-Coleman J, Montgomery J. Rheotaxis revisited: a multi-behavioral and multisensory perspective on how fish orient to flow. J Exp Biol. 2020;223:jeb223008. https://doi.org/10.1242/jeb.223008
Miyata M, Hamaguchi T. Prospects for the gliding mechanism of Mycoplasma mobile. Curr Opin Microbiol. 2016;29:15-21. https://doi.org/10.1016/j.mib.2015.08.010
Balish MF. Mycoplasma pneumoniae, an underutilized model for bacterial cell biology. J Bacteriol. 2014;196:3675-3682. https://doi.org/10.1128/jb.01865-14
Miyata M. Unique centipede mechanism of Mycoplasma gliding. Annu Rev Microbiol. 2010;64:519-537. https://doi.org/10.1146/annurev.micro.112408.134116
Feng M, Schaff AC, Cuadra Aruguete SA, Riggs HE, Distelhorst SL, Balish MF. Development of Mycoplasma pneumoniae biofilms in vitro and the limited role of motility. Int J Med Microbiol. 2018;308:324-334. https://doi.org/10.1016/j.ijmm.2018.01.007
Prince OA, Krunkosky TM, Krause DC. In vitro spatial and temporal analysis of Mycoplasma pneumoniae colonization of human airway epithelium. Infect Immun. 2014;82:579-586. https://doi.org/10.1128/iai.01036-13
Krause DC, Leith DK, Wilson RM, Baseman JB. Identification of Mycoplasma pneumoniae proteins associated with hemadsorption and virulence. Infect Immun. 1982;35:809-817. https://doi.org/10.1128/iai.35.3.809-817.1982
Nakane D, Kabata Y, Nishizaka T. Cell shape controls rheotaxis in small parasitic bacteria. PLoS Pathog. 2022;18:e1010648. https://doi.org/10.1371/journal.ppat.1010648
Miyata M, Robinson RC, Uyeda TQP, et al. Tree of motility-A proposed history of motility systems in the tree of life. Genes Cells. 2020;25:6-21. https://doi.org/10.1111/gtc.12737
Kirchhoff H, Rosengarten R. Isolation of a motile mycoplasma from fish. Microbiology. 1984;130:2439-2445. https://doi.org/10.1099/00221287-130-9-2439
Wadhwa N, Berg HC. Bacterial motility: machinery and mechanisms. Nat Rev Microbiol. 2022;20:161-173. https://doi.org/10.1038/s41579-021-00626-4
Shaevitz JW, Lee JY, Fletcher DA. Spiroplasma swim by a processive change in body helicity. Cell. 2005;122:941-945. https://doi.org/10.1016/j.cell.2005.07.004
Nakane D, Ito T, Nishizaka T. Coexistence of two chiral helices produces kink translation in Spiroplasma swimming. J Bacteriol. 2020;202:e00735-19. https://doi.org/10.1128/JB.00735-19
Sasajima Y, Miyata M. Prospects for the mechanism of Spiroplasma swimming. Front Microbiol. 2021;12:706426. https://doi.org/10.3389/fmicb.2021.706426
Bredt W, Radestock U. Gliding motility of Mycoplasma pulmonis. J Bacteriol. 1977;130:937-938. https://doi.org/10.1128/jb.130.2.937-938.1977
Hatchel JM, Balish MF. Attachment organelle ultrastructure correlates with phylogeny, not gliding motility properties, in Mycoplasma pneumoniae relatives. Microbiology. 2008;154:286-295. https://doi.org/10.1099/mic.0.2007/012765-0
Nakane D, Miyata M. Cytoskeletal asymmetrical dumbbell structure of a gliding mycoplasma, Mycoplasma gallisepticum, revealed by negative-staining electron microscopy. J Bacteriol. 2009;191:3256-3264. https://doi.org/10.1128/jb.01823-08
Relich RF, Friedberg AJ, Balish MF. Novel cellular organization in a gliding mycoplasma, Mycoplasma insons. J Bacteriol. 2009;191:5312-5314. https://doi.org/10.1128/JB.00474-09
Jurkovic DA, Newman JT, Balish MF. Conserved terminal organelle morphology and function in Mycoplasma penetrans and Mycoplasma iowae. J Bacteriol. 2012;194:2877-2883. https://doi.org/10.1128/JB.00060-12
Miyata M, Ryu WS, Berg HC. Force and velocity of Mycoplasma mobile gliding. J Bacteriol. 2002;184:1827-1831. https://doi.org/10.1128/JB.184.7.1827-1831.2002
Nakane D, Miyata M. Cytoskeletal “jellyfish” structure of Mycoplasma mobile. Proc Natl Acad Sci USA. 2007;104:19518-19523. https://doi.org/10.1073/pnas.0704280104
Nelson JB, Lyons MJ. Phase-contrast and electron microscopy of murine strains of Mycoplasma. J Bacteriol. 1965;90:1750-1763. https://doi.org/10.1128/jb.90.6.1750-1763.1965
Sasaki Y. The complete genomic sequence of Mycoplasma penetrans, an intracellular bacterial pathogen in humans. Nucleic Acids Res. 2002;30:5293-5300. https://doi.org/10.1093/nar/gkf667
Jaffe JD, Stange-Thomann N, Smith C, et al. The complete genome and proteome of Mycoplasma mobile. Genome Res. 2004;14:1447-1461. https://doi.org/10.1101/gr.2674004
Wei S, Guo Z, Li T, et al. Genome sequence of Mycoplasma iowae strain 695, an unusual pathogen causing deaths in turkeys. J Bacteriol. 2012;194:547-548. https://doi.org/10.1128/jb.06297-11
Fraser CM, Gocayne JD, White O, et al. The minimal gene complement of Mycoplasma genitalium. Science. 1995;270:397-404. https://doi.org/10.1126/science.270.5235.397
Dandekar T. Re-annotating the Mycoplasma pneumoniae genome sequence: adding value, function and reading frames. Nucleic Acids Res. 2000;28:3278-3288. https://doi.org/10.1093/nar/28.17.3278
Chambaud I. The complete genome sequence of the murine respiratory pathogen Mycoplasma pulmonis. Nucleic Acids Res. 2001;29:2145-2153. https://doi.org/10.1093/nar/29.10.2145
Papazisi L, Gorton TS, Kutish G, et al. The complete genome sequence of the avian pathogen Mycoplasma gallisepticum strain R(low). Microbiology. 2003;149:2307-2316. https://doi.org/10.1099/mic.0.26427-0
Westberg J, Persson A, Holmberg A, et al. The genome sequence of Mycoplasma mycoides subsp. mycoides SC type strain PG1T, the causative agent of contagious bovine pleuropneumonia (CBPP). Genome Res. 2004;14:221-227. https://doi.org/10.1101/gr.1673304
Gillespie SH, Ling CL, Oravcova K, et al. Genomic investigations unmask Mycoplasma amphoriforme, a new respiratory pathogen. Clin Infect Dis. 2015;60:381-388. https://doi.org/10.1093/cid/ciu820
Liu P, Zheng H, Meng Q, et al. Chemotaxis without conventional two-component system, based on cell polarity and aerobic conditions in helicity-switching swimming of Spiroplasma eriocheiris. Front Microbiol. 2017;8:58. https://doi.org/10.3389/fmicb.2017.00058
Weitzman CL, Tillett RL, Sandmeier FC, Tracy CR, Alvarez-Ponce D. High quality draft genome sequence of Mycoplasma testudineum strain BH29(T), isolated from the respiratory tract of a desert tortoise. Stand Genomic Sci. 2018;13:9. https://doi.org/10.1186/s40793-018-0309-z
Andrewes CH, Welch FV. A motile organism of the pleuropneumonia group. J Pathol Bacteriol. 1946;58:578-580. https://doi.org/10.1002/path.1700580333
Baseman JB, Banai M, Kahane I. Sialic acid residues mediate Mycoplasma pneumoniae attachment to human and sheep erythrocytes. Infect Immun. 1982;38:389-391. https://doi.org/10.1128/iai.38.1.389-391.1982
Feldner J, Göbel U, Bredt W. Mycoplasma pneumoniae adhesin localized to tip structure by monoclonal antibody. Nature. 1982;298:765-767. https://doi.org/10.1038/298765a0
Hu PC, Cole RM, Huang YS, et al. Mycoplasma pneumoniae infection: role of a surface protein in the attachment organelle. Science. 1982;216:313-315. https://doi.org/10.1126/science.6801766
Krause DC, Proft T, Hedreyda CT, Hilbert H, Plagens H, Herrmann R. Transposon mutagenesis reinforces the correlation between Mycoplasma pneumoniae cytoskeletal protein HMW2 and cytadherence. J Bacteriol. 1997;179:2668-2677. https://doi.org/10.1128/jb.179.8.2668-2677.1997
Uenoyama A, Kusumoto A, Miyata M. Identification of a 349-kilodalton protein (Gli349) responsible for cytadherence and glass binding during gliding of Mycoplasma mobile. J Bacteriol. 2004;186:1537-1545. https://doi.org/10.1128/jb.186.5.1537-1545.2004
Seto S, Uenoyama A, Miyata M. Identification of a 521-kilodalton protein (Gli521) involved in force generation or force transmission for Mycoplasma mobile gliding. J Bacteriol. 2005;187:3502-3510. https://doi.org/10.1128/jb.187.10.3502-3510.2005
Uenoyama A, Miyata M. Identification of a 123-kilodalton protein (Gli123) involved in machinery for gliding motility of Mycoplasma mobile. J Bacteriol. 2005;187:5578-5584. https://doi.org/10.1128/jb.187.16.5578-5584.2005
Béven L, Charenton C, Dautant A, et al. Specific evolution of F1-like ATPases in Mycoplasmas. PLoS One. 2012;7:e38793. https://doi.org/10.1371/journal.pone.0038793
Cabeen MT, Jacobs-Wagner C. Bacterial cell shape. Nat Rev Microbiol. 2005;3:601-610. https://doi.org/10.1038/nrmicro1205
Takahashi D, Miyata M, Fujiwara I. Assembly properties of bacterial actin MreB involved in Spiroplasma swimming motility. J Biol Chem. 2023;299:104793. https://doi.org/10.1016/j.jbc.2023.104793
Takahashi D, Fujiwara I, Sasajima Y, Narita A, Imada K, Miyata M. ATP-dependent polymerization dynamics of bacterial actin proteins involved in Spiroplasma swimming. Open Biol. 2022;12:220083. https://doi.org/10.1098/rsob.220083
Sasajima Y, Kato T, Miyata T, Kawamoto A, Namba K, Miyata M. Isolation and structure of the fibril protein, a major component of the internal ribbon for Spiroplasma swimming. Front Microbiol. 2022;13:1004601. https://doi.org/10.3389/fmicb.2022.1004601
Kiyama H, Kakizawa S, Sasajima Y, Tahara YO, Miyata M. Reconstitution of a minimal motility system based on Spiroplasma swimming by two bacterial actins in a synthetic minimal bacterium. Sci Adv. 2022;8:eabo7490. https://doi.org/10.1126/sciadv.abo7490
Takahashi D, Fujiwara I, Miyata M. Phylogenetic origin and sequence features of MreB from the wall-less swimming bacteria Spiroplasma. Biochem Biophys Res Commun. 2020;533:638-644. https://doi.org/10.1016/j.bbrc.2020.09.060
Harne S, Duret S, Pande V, Bapat M, Béven L, Gayathri P. MreB5 is a determinant of rod-to-helical transition in the cell-wall-less bacterium Spiroplasma. Curr Biol. 2020;30:4753-4762. https://doi.org/10.1016/j.cub.2020.08.093
Kawamoto A, Matsuo L, Kato T, Yamamoto H, Namba K, Miyata M. Periodicity in attachment organelle revealed by electron cryotomography suggests conformational changes in gliding mechanism of Mycoplasma pneumoniae. mBio. 2016;7:e00243-16. https://doi.org/10.1128/mBio.00243-16
Scheffer MP, Gonzalez-Gonzalez L, Seybert A, et al. Structural characterization of the NAP; the major adhesion complex of the human pathogen Mycoplasma genitalium. Mol Microbiol. 2017;105:869-879. https://doi.org/10.1111/mmi.13743
Nishikawa MS, Nakane D, Toyonaga T, et al. Refined mechanism of Mycoplasma mobile gliding based on structure, ATPase activity, and sialic acid binding of machinery. mBio. 2019;10: 10-1128. https://doi.org/10.1128/mBio.02846-19
Tanaka A, Nakane D, Mizutani M, Nishizaka T, Miyata M. Directed binding of gliding bacterium, Mycoplasma mobile, shown by detachment force and bond lifetime. mBio. 2016;7:e00455-16. https://doi.org/10.1128/mBio.00455-16
Mizutani M, Tulum I, Kinosita Y, Nishizaka T, Miyata M. Detailed analyses of stall force generation in Mycoplasma mobile gliding. Biophys J. 2018;114:1411-1419. https://doi.org/10.1016/j.bpj.2018.01.029
Mizutani M, Sasajima Y, Miyata M. Force and stepwise movements of gliding motility in human pathogenic bacterium Mycoplasma pneumoniae. Front Microbiol. 2021;12:747905. https://doi.org/10.3389/fmicb.2021.747905
Hasselbring BM, Krause DC. Cytoskeletal protein P41 is required to anchor the terminal organelle of the wall-less prokaryote Mycoplasma pneumoniae. Mol Microbiol. 2007;63:44-53. https://doi.org/10.1111/j.1365-2958.2006.05507.x
Nakane D, Miyata M. Mycoplasma mobile cells elongated by detergent and their pivoting movements in gliding. J Bacteriol. 2012;194:122-130. https://doi.org/10.1128/jb.05857-11
Nakane D, Adan-Kubo J, Kenri T, Miyata M. Isolation and characterization of P1 adhesin, a leg protein of the gliding bacterium Mycoplasma pneumoniae. J Bacteriol. 2011;193:715-722. https://doi.org/10.1128/JB.00796-10
Aparicio D, Torres-Puig S, Ratera M, et al. Mycoplasma genitalium adhesin P110 binds sialic-acid human receptors. Nat Commun. 2018;9:4471. https://doi.org/10.1038/s41467-018-06963-y
Vizarraga D, Kawamoto A, Matsumoto U, et al. Immunodominant proteins P1 and P40/P90 from human pathogen Mycoplasma pneumoniae. Nat Commun. 2020;11:5188. https://doi.org/10.1038/s41467-020-18777-y
Henderson GP, Jensen GJ. Three-dimensional structure of Mycoplasma pneumoniae's attachment organelle and a model for its role in gliding motility. Mol Microbiol. 2006;60:376-385. https://doi.org/10.1111/j.1365-2958.2006.05113.x
Seybert A, Herrmann R, Frangakis AS. Structural analysis of Mycoplasma pneumoniae by cryo-electron tomography. J Struct Biol. 2006;156:342-354. https://doi.org/10.1016/j.jsb.2006.04.010
Nakane D, Kenri T, Matsuo L, Miyata M. Systematic structural analyses of attachment organelle in Mycoplasma pneumoniae. PLoS Pathog. 2015;11:e1005299. https://doi.org/10.1371/journal.ppat.1005299
Kawakita Y, Kinoshita M, Furukawa Y, et al. Structural study of MPN387, an essential protein for gliding motility of a human-pathogenic bacterium, Mycoplasma pneumoniae. J Bacteriol. 2016;198:2352-2359. https://doi.org/10.1128/jb.00160-16
Nakane D, Murata K, Kenri T, Shibayama K, Nishizaka T. Molecular ruler of the attachment organelle in Mycoplasma pneumoniae. PLoS Pathog. 2021;17:e1009621. https://doi.org/10.1371/journal.ppat.1009621
Adan-Kubo J, Uenoyama A, Arata T, Miyata M. Morphology of isolated Gli349, a leg protein responsible for Mycoplasma mobile gliding via glass binding, revealed by rotary shadowing electron microscopy. J Bacteriol. 2006;188:2821-2828. https://doi.org/10.1128/jb.188.8.2821-2828.2006
Nonaka T, Adan-Kubo J, Miyata M. Triskelion structure of the Gli521 protein, involved in the gliding mechanism of Mycoplasma mobile. J Bacteriol. 2010;192:636-642. https://doi.org/10.1128/jb.01143-09
Matsuike D, Tahara YO, Nonaka T, et al. Structure and function of Gli123 involved in Mycoplasma mobile gliding. J Bacteriol. 2023;205:e0034022. https://doi.org/10.1128/jb.00340-22
Tulum I, Yabe M, Uenoyama A, Miyata M. Localization of P42 and F(1)-ATPase α-subunit homolog of the gliding machinery in Mycoplasma mobile revealed by newly developed gene manipulation and fluorescent protein tagging. J Bacteriol. 2014;196:1815-1824. https://doi.org/10.1128/jb.01418-13
Tulum I, Kimura K, Miyata M. Identification and sequence analyses of the gliding machinery proteins from Mycoplasma mobile. Sci Rep. 2020;10:3792. https://doi.org/10.1038/s41598-020-60535-z
Kobayashi K, Kodera N, Kasai T, et al. Movements of Mycoplasma mobile gliding machinery detected by high-speed atomic force microscopy. mBio. 2021;12:e0004021. https://doi.org/10.1128/mBio.00040-21
Toyonaga T, Kato T, Kawamoto A, et al. Chained structure of dimeric F1-like ATPase in Mycoplasma mobile gliding machinery. mBio. 2021;12:e01414-e01421. https://doi.org/10.1128/mBio.01414-21
Balish MF. Giant steps toward understanding a mycoplasma gliding motor. TIM. 2014;22:429-431. https://doi.org/10.1016/j.tim.2014.06.005
Kinosita Y, Nakane D, Sugawa M, et al. Unitary step of gliding machinery in Mycoplasma mobile. Proc Natl Acad Sci USA. 2014;111:8601-8606. https://doi.org/10.1073/pnas.1310355111
Wadhams GH, Armitage JP. Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol. 2004;5:1024-1037. https://doi.org/10.1038/nrm1524
Morio H, Kasai T, Miyata M. Gliding direction of Mycoplasma mobile. J Bacteriol. 2016;198:283-290. https://doi.org/10.1128/JB.00499-15
Waites KB, Xiao L, Liu Y, Balish MF, Atkinson TP. Mycoplasma pneumoniae from the respiratory tract and beyond. Clin Microbiol Rev. 2017;30:747-809. https://doi.org/10.1128/CMR.00114-16
Lo SC, Hayes MM, Tully JG, et al. Mycoplasma penetrans sp. nov., from the urogenital tract of patients with AIDS. Int J Syst Bacteriol. 1992;42:357-364. https://doi.org/10.1099/00207713-42-3-357
Dufrêne YF, Persat A. Mechanomicrobiology: how bacteria sense and respond to forces. Nat Rev Microbiol. 2020;18:227-240. https://doi.org/10.1038/s41579-019-0314-2
Laventie B-J, Jenal U. Surface sensing and adaptation in bacteria. Annu Rev Microbiol. 2020;74:735-760.
Marcos, Fu HC, Powers TR, Stocker R. Bacterial rheotaxis. Proc Natl Acad Sci USA. 2012;109:4780-4785. https://doi.org/10.1073/pnas.1120955109
Rusconi R, Stocker R. Microbes in flow. Curr Opin Microbiol. 2015;25:1-8. https://doi.org/10.1016/j.mib.2015.03.003
Padron GC, Shuppara AM, Palalay J-JS, Sharma A, Sanfilippo JE. Bacteria in fluid flow. J Bacteriol. 2023;205:e00400-e00422. https://doi.org/10.1128/jb.00400-22
Kantsler V, Dunkel J, Blayney M, Goldstein RE. Rheotaxis facilitates upstream navigation of mammalian sperm cells. eLife. 2014;3:e02403. https://doi.org/10.7554/eLife.02403
Nishigami Y, Ohmura T, Taniguchi A, et al. Influence of cellular shape on sliding behavior of ciliates. Commun Integr Biol. 2018;11:e1506666. https://doi.org/10.1080/19420889.2018.1506666
Ohmura T, Nishigami Y, Taniguchi A, et al. Simple mechanosense and response of cilia motion reveal the intrinsic habits of ciliates. Proc Natl Acad Sci USA. 2018;115:3231-3236. https://doi.org/10.1073/pnas.1718294115
Ohmura T, Nishigami Y, Taniguchi A, Nonaka S, Ishikawa T, Ichikawa M. Near-wall rheotaxis of the ciliate Tetrahymena induced by the kinesthetic sensing of cilia. Sci Adv. 2021;7:eabi5878. https://doi.org/10.1126/sciadv.abi5878
Omori T, Kikuchi K, Schmitz M, Pavlovic M, Chuang CH, Ishikawa T. Rheotaxis and migration of an unsteady microswimmer. J Fluid Mech. 2022;930:A30. https://doi.org/10.1017/jfm.2021.921
Kaya T, Koser H. Direct upstream motility in Escherichia coli. Biophys J. 2012;102:1514-1523. https://doi.org/10.1016/j.bpj.2012.03.001
Mathijssen AJTM, Figueroa-Morales N, Junot G, Clément É, Lindner A, Zöttl A. Oscillatory surface rheotaxis of swimming E. coli bacteria. Nat Commun. 2019;10:3434. https://doi.org/10.1038/s41467-019-11360-0
Jing G, Zöttl A, Clément É, Lindner A. Chirality-induced bacterial rheotaxis in bulk shear flows. Sci Adv. 2020;6:eabb2012. https://doi.org/10.1126/sciadv.abb2012
Meng Y, Li Y, Galvani CD, et al. Upstream migration of Xylella fastidiosa via pilus-driven twitching motility. J Bacteriol. 2005;187:5560-5567. https://doi.org/10.1128/jb.187.16.5560-5567.2005
Shen Y, Siryaporn A, Lecuyer S, Gitai Z, Stone HA. Flow directs surface-attached bacteria to twitch upstream. Biophys J. 2012;103:146-151. https://doi.org/10.1016/j.bpj.2012.05.045
Persat A, Stone HA, Gitai Z. The curved shape of Caulobacter crescentus enhances surface colonization in flow. Nat Commun. 2014;5:3824. https://doi.org/10.1038/ncomms4824
Siryaporn A, Kim MK, Shen Y, Stone HA, Gitai Z. Colonization, competition, and dispersal of pathogens in fluid flow networks. Curr Biol. 2015;25:1201-1207. https://doi.org/10.1016/j.cub.2015.02.074
Palacci J, Sacanna S, Abramian A, et al. Artificial rheotaxis. Sci Adv. 2015;1:e1400214. https://doi.org/10.1126/sciadv.1400214
McBride MJ, Nakane D. Flavobacterium gliding motility and the type IX secretion system. Curr Opin Microbiol. 2015;28:72-77. https://doi.org/10.1016/j.mib.2015.07.016
Nan B, Zusman DR. Novel mechanisms power bacterial gliding motility. Mol Microbiol. 2016;101:186-193. https://doi.org/10.1111/mmi.13389
Bustamante-Marin XM, Ostrowski LE. Cilia and mucociliary clearance. Cold Spring Harbor Perspect Biol. 2017;9:a028241. https://doi.org/10.1101/cshperspect.a028241
Zheng S, Carugo D, Mosayyebi A, et al. Fluid mechanical modeling of the upper urinary tract. WIREs Mech Dis. 2021;13:e1523. https://doi.org/10.1002/wsbm.1523
Wilson JM, Laurent P. Fish gill morphology: inside out. J Exp Zool. 2002;293:192-213. https://doi.org/10.1002/jez.10124
Hofmann W. The effect of lung structure on mucociliary clearance and particle retention in human and rat lungs. Toxicol Sci. 2003;73:448-456. https://doi.org/10.1093/toxsci/kfg075
Hill DB, Swaminathan V, Estes A, et al. Force generation and dynamics of individual cilia under external loading. Biophys J. 2010;98:57-66. https://doi.org/10.1016/j.bpj.2009.09.048
Hughes GM. The dimensions of fish gills in relation to their function. J Exp Biol. 1966;45:177-195. https://doi.org/10.1242/jeb.45.1.177
Gurung JP, Gel M, Baker MAB. Microfluidic techniques for separation of bacterial cells via taxis. Microb Cell. 2020;7:66-79. https://doi.org/10.15698/mic2020.03.710