Physical Microbiology PDF
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Advances in Experimental Medicine and Biology 1267 Guillaume Duménil Sven van Teeffelen Editors Physical Microbiology Advances in Experimental Medicine and Biology Volume 1267 SeriesEditors WimE.Crusio,InstitutdeNeurosciencesCognitivesetIntégrativesd’Aquitaine, CNRSandUniversityofBordeauxUMR5287,PessacCedex,France HaidongDong,DepartmentsofUrologyandImmunology,MayoClinic, Rochester,MN,USA HeinfriedH.Radeke,InstituteofPharmacology&Toxicology,Clinicofthe GoetheUniversityFrankfurtMain,FrankfurtamMain,Hessen,Germany NimaRezaei,ResearchCenterforImmunodeficiencies,Children’sMedical Center,TehranUniversityofMedicalSciences,Tehran,Iran Advances in Experimental Medicine and Biology provides a platform for scientificcontributionsinthemaindisciplinesofthebiomedicineandthelife sciences. This series publishes thematic volumes on contemporary research in the areas of microbiology, immunology, neurosciences, biochemistry, biomedicalengineering,genetics,physiology,andcancerresearch.Covering emergingtopicsandtechniquesinbasicandclinicalscience,itbringstogether cliniciansandresearchersfromvariousfields. Advances in Experimental Medicine and Biology has been publishing exceptionalworksinthefieldforover40years,andisindexedinSCOPUS, Medline (PubMed), Journal Citation Reports/Science Edition, Science Citation Index Expanded (SciSearch, Web of Science), EMBASE, BIOSIS, Reaxys, EMBiology, the Chemical Abstracts Service (CAS), and Pathway Studio. 2019ImpactFactor:2.4505YearImpactFactor:2.324 Moreinformationaboutthisseriesathttp://www.springer.com/series/5584 Guillaume Duménil • Sven van Teeffelen Editors Physical Microbiology Editors GuillaumeDuménil SvenvanTeeffelen PathogenesisofVascularInfections MicrobialMorphogenesisandGrowth InstitutPasteur InstitutPasteur Paris,France Paris,France ISSN0065-2598 ISSN2214-8019 (electronic) AdvancesinExperimentalMedicineandBiology ISBN978-3-030-46885-9 ISBN978-3-030-46886-6 (eBook) https://doi.org/10.1007/978-3-030-46886-6 ©SpringerNatureSwitzerlandAG2020 Thisworkissubjecttocopyright.AllrightsarereservedbythePublisher,whetherthewhole orpartofthematerialisconcerned,specificallytherightsoftranslation,reprinting,reuseof illustrations,recitation,broadcasting,reproductiononmicrofilmsorinanyotherphysicalway, andtransmissionorinformationstorageandretrieval,electronicadaptation,computersoftware, orbysimilarordissimilarmethodologynowknownorhereafterdeveloped. Theuseofgeneraldescriptivenames,registerednames,trademarks,servicemarks,etc.inthis publicationdoesnotimply,evenintheabsenceofaspecificstatement,thatsuchnamesare exemptfromtherelevantprotectivelawsandregulationsandthereforefreeforgeneraluse. Thepublisher,theauthors,andtheeditorsaresafetoassumethattheadviceandinformationin thisbookarebelievedtobetrueandaccurateatthedateofpublication.Neitherthepublisher northeauthorsortheeditorsgiveawarranty,expressedorimplied,withrespecttothematerial containedhereinorforanyerrorsoromissionsthatmayhavebeenmade.Thepublisherremains neutralwithregardtojurisdictionalclaimsinpublishedmapsandinstitutionalaffiliations. ThisSpringerimprintispublishedbytheregisteredcompanySpringerNatureSwitzerlandAG. Theregisteredcompanyaddressis:Gewerbestrasse11,6330Cham,Switzerland Preface Macroscopic phenomena in biology are the result of the complex interplay of many stochastically interacting microscopic proteins and molecules. To understandhowmacroscopicbehaviorcomesaboutfrommicroscopicinter- actions, we have to build quantitative physical models. While this concept has been understood in developmental and also in eukaryotic cell biology, bacteria have long been regarded as “bags of enzymes” that do not provide complex multi-scale self-organization. However, with increasing technical possibilities to observe and quantify bacterial behavior and bacterial cell biology, this point of view has slowly changed. Today, there are multiple bacterial subsystems that have profited from physical approaches, notably theflagellarmotor,thecellenvelope,thechromosome,andosmoticpressure. Other,morecomplexsystemsorsetsofsystems,suchasbacterialvirulence, arealsounderinvestigationwithapproachesfromphysics. The contents of the book intend to illustrate this trend of approaching questionsofself-organizationinbacterialmicrobiologywithapproachesfrom physics, which we refer to as Physical microbiology. This book attempts to presentrecentconceptsandtoolsinthisemergingfield.Chaptersarewritten tobeofinteresttobiologists,whowishtoaddconceptsandtoolsfromphysics totheirresearchandforphysicistswhowishtoexplorebiologicalprocesses. A set of technical developments shed a new light on all aspects of microbiology, basic bacterial physiology, and division but also on issues relatedtoinfection,throughantibioticsresistance,virulencefactors,andhost response to infection. Video microscopy is of particular interest here as it allowstofollowspecificallylabelledproteinsinspaceandtime.Microscopes andcamerasofvideomicroscopesnowallowtoreachresolutionscompatible withobservationsofspecificcomponentsinsidebacteriaanddeterminetheir positionrelativetomajorbacterialcomponentssuchasmembrane,nucleoid, or bacterial poles. Microfluidics-based approaches to confine or constrain bacteria provide a powerful tool in combination with video-microscopy. Super-resolutionmicroscopytakestheseobservationsanextrastepfurtherin resolution. Finally, cryo-electron microscopy combined with single-particle averagingbringsamolecular-levelview. A key feature of the techniques described above is the ability to extract quantitativeinformation.Biologicalobjectsofinterestcanbecounted,their size measured, and their speed determined in the case of video microscopy. Thisquantitativeaspectiscriticalasitallowsconfrontationwithphysicallaws v vi Preface andtestingofspecificphysicalmodelsleadingtovalidationorinvalidation.In mostinstancesthereisanecessitytorevisitphysicstoaddressthesespecific questions. Together, physics and quantitative observation provide a novel visionofmicrobiology. ThebookstartswithachapterbyEnriqueRojasthatexploresanddescribes the mechanical properties of bacteria. This chapter highlights the role of different cell-envelope components, the bacterial cytoskeleton, and of the nucleoid. The main mode of transport in bacteria is diffusion. The chapter byChristopherH.BohrerandJieXiaoisdevotedtocharacterizingdiffusion ofproteinsinbacteria,andtothedifferenttoolstomeasurediffusion,witha focusonsingle-moleculetracking.Oneofthemaintasksofbacteriaduring every generation of growth is the faithful replication and segregation of their DNA. Antoine Le Gall and Marcelo Nollmann describe the physical mechanism underlying chromosome and plasmid segregation through the ParABSsystem.LeGallandNollmanndemonstratethatthesystemdisplays complex dynamics, and its understanding requires physical modeling. Ines Baptistaandcolleaguesgiveanoverviewofthespatialdistributionofdifferent cellularcomponents,andtheyprovideevidencethatthenucleoidhasamajor organizingfunctioninbacteria.Bacteriacontainremarkablycomplexmulti- componentmachinessuchassecretionsystemsandflagellarmotors.Ashley NordandFrancescoPedacidescribethecomplexityofthebacterialflagellar motor and its implications for physical function. During infection, bacterial pathogensinteractwiththeirhostinavarietyofwaysincludingthroughthe secretion of toxins. David Gonzalez-Rodriguez and colleagues explore the physical principles that allow certain toxins to form large openings through hostcells.Finally,ToryDoolinandcolleaguesreviewcurrentknowledgeon amechanismofbacterialkillingbyhistonesfromeukaryoticcells. The contents of these chapters are intended to provide a state-of-the- art view of the emerging field of physical microbiology for biologists and physicists.Weareconvincedofthehugepotentialofthisfieldbothinterms of basic and applied sciences and we hope this book will be a source of inspirationforstudentsandresearchers. Paris,France GuillaumeDuménil Paris,France SvenvanTeeffelen Contents 1 TheMechanicalPropertiesofBacteriaandWhy theyMatter ............................................. 1 EnriqueR.Rojas 2 ComplexDiffusioninBacteria ............................ 15 ChristopherH.BohrerandJieXiao 3 PhysicalViewsonParABS-MediatedDNASegregation ...... 45 BaptisteGuilhas,AntoineLe Gall,andMarcelloNollmann 4 EfficiencyandRobustnessofProcessesDrivenbyNucleoid ExclusioninEscherichiacoli .............................. 59 Ines Baptista, Vatsala Chauhan, Bilena Almeida, VinodhKandavalli,andAndreS.Ribeiro 5 MechanismsandDynamicsoftheBacterialFlagellarMotor.. 81 A.L.NordandFPedaci 6 Dewetting:FromPhysicstotheBiologyofIntoxicatedCells .. 101 DavidGonzalez-Rodriguez,CamilleMorel, andEmmanuelLemichez 7 PhysicalMechanismsofBacterialKillingbyHistones........ 117 ToryDoolin,StevenGross,andAlbertSiryaporn Index ...................................................... 135 vii 1 The Mechanical Properties of Bacteria and Why they Matter EnriqueR.Rojas “Itbehoovesusalwaystorememberthatinphysicsithastakengreatscientiststo discoversimplethings.Theyareverygreatnamesindeedwhichwecouplewiththe explanationofthepathofastone,thedroopofachain,thetintsofabubble,the shadowsinacup.Itisbuttheslightestadumbrationofadynamicalmorphology[of biologicalsystems]thatwecanhopetohaveuntilthephysicistandthemathematician shallhavemadetheseproblemsofourstheirown.” –D’arcyThompson,OnGrowthandForm. Abstract 1.1 Introduction Ireviewrecenttechniquestomeasuretheme- chanicalpropertiesofbacterialcellsandtheir Bacteriaarethesmallest,simplest,andmostsuc- subcellularcomponents,andthendiscusswhat cessful (that is, most numerous) class of living thesetechniqueshaverevealedaboutthecon- organisms on Earth. It is reasonable to assume stitutive mechanical properties of whole bac- that these three traits are intimately connected terialcellsandsubcellularmaterial,aswellas witheachother,andwithbacteria’sfoundational themolecularbasisfortheseproperties. role in our understanding of molecular biology. However, these traits have historically been “se- lectedagainst”bythoseinterestedinbiomechan- ics: their small size renders bacterial cells in- tractabletomanybiophysicalassaysusedoneu- Keywords karyoticcellsortissues,andtheirrelativesimplic- Mechanobiology·Cellgrowth·Cellular ity(forexample,theirlackofatruecytoskeleton) morphogenesis alongwithahistoricalfocusontheirgeneticsand molecularbiologyhaveperhapscausedscientists tounderestimatetherichnessoftheirmechanics andthevalueofstudyingthem. E.R.Rojas((cid:2)) Overthelast10yearstherehasbeenarealiza- DepartmentofBiology,NewYorkUniversity,NewYork, NY,USA tionoftheimportanceofmechanicalsensingand e-mail:[email protected] signaling in bacteria (reviewed elsewhere in this ©SpringerNatureSwitzerlandAG2020 1 G.Duménil,S.vanTeeffelen(eds.),PhysicalMicrobiology,AdvancesinExperimentalMedicine andBiology1267,https://doi.org/10.1007/978-3-030-46886-6_1 2 E.R.Rojas volume; also see Persat et al. 2015). In parallel, severalfundamentalmeasurementshavebegunto magnitude of mechanical stresses applied elucidatetheintriguingmechanicalpropertiesof toit. bacterial cells. Due to the size of bacteria, these Elastic: Possesses the simplest con- measurementshavetypicallyrequiredHerculean stitutive relationship for a solid material efforts in assay development to make what in which strain is proportional to stress, are relatively crude mechanical measurements σ=Eε,anddeformationisreversiblewhen comparedtowhatcanbemeasuredforeukaryotic the force is removed. E is the “Young’s cells or non-living materials. Yet these seminal Modulus”andhasdimensionsofpressure. measurements have already demonstrated that Nonlinearelastic:Possessesaconstitu- bacteria possess many novel materials from tive relationship in which deformation in- a mechanics perspective, and underscore the creases with applied stress but not propor- importance of endeavoring to characterize these tionally. materials. Strain-stiffening: A specific type of While the field of bacterial cell mechanics nonlinearelasticityinwhichtheamountof is still in its infancy, in certain cases it is clear additionalforcerequiredtostretchamate- how the mechanical properties of subcellular rialagivenamountincreasesasthematerial material are adaptive with respect to subcellular isstretched. physiologicalprocessesorsurvivalofthecellin Viscoelastic: Has properties of both a complexenvironments.Here,Iwillreviewwhat solid and a liquid. A viscoelastic material wehavelearnedaboutthemechanicalproperties behavesasasolidimmediatelyafterastress of bacteria, beginning with measurements of is applied, but flows like a liquid after whole-cellmechanicalpropertiesandproceeding longerperiods. to those of each subcellular material. Instead of Plastic: Deforms irreversibly if the ap- simply listing the absolute quantitative values pliedstressexceedsacertainthresholdoris of mechanical properties (stiffness, viscosity, appliedforlongenough.Aplasticmaterial etc.), I will focus on discussing the constitutive isasolid. properties (Box 1.1) of the cell and its Glass:Amaterialthatbehavesasavis- subcellularmaterials,thatis,thefunctionalform cousliquidorrubberymaterialaboveacer- ofthequantitativedependenceofthedeformation tain critical temperature and a brittle solid ofamaterialontheforcesappliedtoit.Alongthe belowit. way,Iwillhighlightthecurrentmethodsavailable Anisotropic: Possesses different struc- for assaying bacterial mechanics. Finally, in turalandmechanicalpropertiesindifferent each case, I will discuss the relevance of the directions. mechanicalpropertiestocellularphysiology. Flexural Rigidity (κ): The degree to whichamaterial(likeacell)resistsbending Box1.1:ABriefGlossaryofMechanics when a deflection force is applied to it. MechanicalStress(σ):Aforcedistributed Flexural rigidity has dimensions of force timesarea. overanarea.Stresshasdimensionsofpres- sure. Mechanical Strain (ε): The degree to whichamaterialisstretched.Strainhasno 1.2 MechanicalElements dimensions – it is a fractional change in oftheBacterialCell length,areaorvolume. Constitutive property: The specific, Mostreadersofthischapterwillbefamiliarwith quantitativerelationshipbetweenthemag- the structural components of the bacterial cell. nitudeofdeformationofamaterialandthe I will briefly outline the bacterial cell features relevanttothetopicofmechanics.
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