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      Cell shape controls rheotaxis in small parasitic bacteria

      research-article
      1 , * , , 2 , 2 , * ,
      PLoS Pathogens
      Public Library of Science

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          Abstract

          Mycoplasmas, a group of small parasitic bacteria, adhere to and move across host cell surfaces. The role of motility across host cell surfaces in pathogenesis remains unclear. Here, we used optical microscopy to visualize rheotactic behavior in three phylogenetically distant species of Mycoplasma using a microfluidic chamber that enabled the application of precisely controlled fluid flow. We show that directional movements against fluid flow occur synchronously with the polarized cell orienting itself to be parallel against the direction of flow. Analysis of depolarized cells revealed that morphology itself functions as a sensor to recognize rheological properties that mimic those found on host-cell surfaces. These results demonstrate the vital role of cell morphology and motility in responding to mechanical forces encountered in the native environment.

          Author summary

          The small, parasitic bacterium Mycoplasma pneumoniae attaches to, and moves over, host cell surfaces. Adherence to host surfaces and motility are critical for the pathogenicity of M. pneumoniae. The role of motility by M. pneumoniae in vivo, however, is poorly understood. Host airways generate constant fluid flow toward the mouth as part of their defense against pathogens and irritants. Consequently, pulmonary invaders must counter the rheological forces found in host airways in order to successfully colonize the host. Here, we demonstrate that M. pneumoniae exhibits directional movement against fluid flow. These findings suggest there is a vital role for rheotactic motility that has evolved in order to overcome host defense mechanisms such as mucociliary clearance.

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          Most cited references63

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          NIH Image to ImageJ: 25 years of image analysis

          For the past twenty five years the NIH family of imaging software, NIH Image and ImageJ have been pioneers as open tools for scientific image analysis. We discuss the origins, challenges and solutions of these two programs, and how their history can serve to advise and inform other software projects.
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            Feature point tracking and trajectory analysis for video imaging in cell biology.

            This paper presents a computationally efficient, two-dimensional, feature point tracking algorithm for the automated detection and quantitative analysis of particle trajectories as recorded by video imaging in cell biology. The tracking process requires no a priori mathematical modeling of the motion, it is self-initializing, it discriminates spurious detections, and it can handle temporary occlusion as well as particle appearance and disappearance from the image region. The efficiency of the algorithm is validated on synthetic video data where it is compared to existing methods and its accuracy and precision are assessed for a wide range of signal-to-noise ratios. The algorithm is well suited for video imaging in cell biology relying on low-intensity fluorescence microscopy. Its applicability is demonstrated in three case studies involving transport of low-density lipoproteins in endosomes, motion of fluorescently labeled Adenovirus-2 particles along microtubules, and tracking of quantum dots on the plasma membrane of live cells. The present automated tracking process enables the quantification of dispersive processes in cell biology using techniques such as moment scaling spectra.
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              Mycoplasma pneumoniae from the Respiratory Tract and Beyond.

              Mycoplasma pneumoniae is an important cause of respiratory tract infections in children as well as adults that can range in severity from mild to life-threatening. Over the past several years there has been much new information published concerning infections caused by this organism. New molecular-based tests for M. pneumoniae detection are now commercially available in the United States, and advances in molecular typing systems have enhanced understanding of the epidemiology of infections. More strains have had their entire genome sequences published, providing additional insights into pathogenic mechanisms. Clinically significant acquired macrolide resistance has emerged worldwide and is now complicating treatment. In vitro susceptibility testing methods have been standardized, and several new drugs that may be effective against this organism are undergoing development. This review focuses on the many new developments that have occurred over the past several years that enhance our understanding of this microbe, which is among the smallest bacterial pathogens but one of great clinical importance.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: Methodology
                Role: ConceptualizationRole: Funding acquisition
                Role: Editor
                Journal
                PLoS Pathog
                PLoS Pathog
                plos
                PLoS Pathogens
                Public Library of Science (San Francisco, CA USA )
                1553-7366
                1553-7374
                14 July 2022
                July 2022
                : 18
                : 7
                : e1010648
                Affiliations
                [1 ] Department of Engineering Science, Graduate School of Informatics and Engineering, The University of Electro-Communications, Tokyo, Japan
                [2 ] Department of Physics, Gakushuin University, Tokyo, Japan
                Miami University, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0002-8201-2608
                Article
                PPATHOGENS-D-22-00431
                10.1371/journal.ppat.1010648
                9282661
                35834494
                da9bb42d-0366-40bf-b9c2-c2682d454d21
                © 2022 Nakane et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 9 March 2022
                : 6 June 2022
                Page count
                Figures: 5, Tables: 0, Pages: 14
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 22H05066
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 21K07020
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 20H05543
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004051, Kato Memorial Bioscience Foundation;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100007428, Naito Foundation;
                Award Recipient :
                Funded by: Noguchi Institute
                Award Recipient :
                This study was supported partly by KAKENHI grants from the Japan Society for the Promotion of Science (22H05066, 21K07020, and 20H05543 to D.N.) and funds from the Kato Memorial Bioscience Foundation, the Naito Foundation, and the Noguchi Institute to D.N. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Physical Sciences
                Physics
                Classical Mechanics
                Continuum Mechanics
                Fluid Mechanics
                Fluid Dynamics
                Fluid Flow
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Mycoplasma Pneumoniae
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Mycoplasma Pneumoniae
                Biology and Life Sciences
                Organisms
                Bacteria
                Mollicutes
                Mycoplasma
                Mycoplasma Pneumoniae
                Biology and Life Sciences
                Cell Biology
                Cell Motility
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Virulence Factors
                Pathogen Motility
                Biology and Life Sciences
                Organisms
                Bacteria
                Mollicutes
                Mycoplasma
                Physical Sciences
                Physics
                Classical Mechanics
                Motion
                Velocity
                Biology and Life Sciences
                Cell Biology
                Cellular Structures and Organelles
                Research and Analysis Methods
                Microscopy
                Electron Microscopy
                Custom metadata
                All relevant data are within the manuscript and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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