The Mechanical World of Bacteria
2015; Cell Press; Volume: 161; Issue: 5 Linguagem: Inglês
10.1016/j.cell.2015.05.005
ISSN1097-4172
AutoresAlexandre Persat, Carey D. Nadell, Minyoung Kevin Kim, François Ingremeau, Albert Siryaporn, Knut Drescher, Ned S. Wingreen, Bonnie L. Bassler, Zemer Gitai, Howard A. Stone,
Tópico(s)Bacteriophages and microbial interactions
ResumoIn the wild, bacteria are predominantly associated with surfaces as opposed to existing as free-swimming, isolated organisms. They are thus subject to surface-specific mechanics, including hydrodynamic forces, adhesive forces, the rheology of their surroundings, and transport rules that define their encounters with nutrients and signaling molecules. Here, we highlight the effects of mechanics on bacterial behaviors on surfaces at multiple length scales, from single bacteria to the development of multicellular bacterial communities such as biofilms. In the wild, bacteria are predominantly associated with surfaces as opposed to existing as free-swimming, isolated organisms. They are thus subject to surface-specific mechanics, including hydrodynamic forces, adhesive forces, the rheology of their surroundings, and transport rules that define their encounters with nutrients and signaling molecules. Here, we highlight the effects of mechanics on bacterial behaviors on surfaces at multiple length scales, from single bacteria to the development of multicellular bacterial communities such as biofilms. Bacteria occupy a broad variety of ecological niches on Earth. Their long evolutionary history has exposed them to vastly different environments, and they have evolved remarkable plasticity in response to locally changing physicochemical conditions. In particular, bacteria can detect and respond to chemical, thermal, and mechanical cues, as well as to electric and magnetic fields. How do these cues influence bacterial behaviors in natural environments? Characterizing bacterial behavior in realistic contexts requires integrating a spectrum of environmental stimuli to which they respond and doing so in physical configurations representative of their natural habitats. Such analyses are critical to comprehensively understand bacterial biology and to thereby make progress in promoting or restricting bacterial growth in medical, industrial, and agricultural realms. Mechanics is an integral part of eukaryotic cell biology: numerous studies have demonstrated the importance of fluid flow and surface mechanics in mammalian cell growth and behavior at many length scales (Fritton and Weinbaum, 2009Fritton S.P. Weinbaum S. Fluid and solute transport in bone: flow-induced mechanotransduction.Annu. Rev. Fluid Mech. 2009; 41: 347-374Crossref PubMed Scopus (266) Google Scholar, Hoffman et al., 2011Hoffman B.D. Grashoff C. Schwartz M.A. Dynamic molecular processes mediate cellular mechanotransduction.Nature. 2011; 475: 316-323Crossref PubMed Scopus (681) Google Scholar, Pruitt et al., 2014Pruitt B.L. Dunn A.R. Weis W.I. Nelson W.J. Mechano-transduction: from molecules to tissues.PLoS Biol. 2014; 12: e1001996Crossref PubMed Scopus (53) Google Scholar). In contrast, microbiology has traditionally focused on the influence of the chemical environment on bacterial behavior. Hence, for decades, growth in well-mixed batch cultures and on agar plates were the methods of choice for studies of bacterial physiology. As a result, the community has only recently recognized that mechanics also play a significant role in microbial biology on surfaces—fluid flow and contact between cells and surfaces are two ubiquitous and influential features of bacterial existence in natural environments. Advances in microscale engineering and microscopy now provide us with powerful tools to explore, at the relevant spatial scales, the roles physical forces play in bacterial sensory perception and adaptation (Rusconi et al., 2014Rusconi R. Garren M. Stocker R. Microfluidics expanding the frontiers of microbial ecology.Annu. Rev. Biophys. 2014; 43: 65-91Crossref PubMed Scopus (133) Google Scholar). These new experimental platforms have revealed that bacteria are attuned to mechanical forces and, indeed, can exploit mechanics to drive adaptive behavior. Swimming motility provides an elegant example of how bacteria are influenced by the mechanical nature of their surroundings. As a consequence of their small size (∼1 μm), bacteria live in environments dominated by viscosity, which stands in contrast to the meter-scale world of humans in which dynamics are dominated by inertia (Purcell, 1977Purcell E.M. Life at low Reynolds-number.Am. J. Phys. 1977; 45: 3-11Crossref Scopus (2958) Google Scholar). Fluid motion can be broadly characterized by the Reynolds number (Re), which compares the magnitudes of inertial forces and viscous forces in a given flow (Re = ρUL/μ where U is a typical fluid speed, L a typical length scale, ρ the density of the fluid, and μ its viscosity). We humans live a high Reynolds number life (at least 104), as we are meter-scale organisms moving at speeds on the order of meters per second. But swimming microorganisms live at Reynolds numbers far below unity (at most 10−3). To self-propel in such a regime, bacteria use motorized flagella that convert mechanical actuation (rotation) into net displacement. Thus, many bacteria have evolved a biological machine—the flagellum and its associated motor—to adapt to the mechanical properties of their (purely viscous) environment. The biology and physics of swimming motility have been intensively investigated and are reviewed elsewhere (Berg, 2003Berg H.C. The rotary motor of bacterial flagella.Annu. Rev. Biochem. 2003; 72: 19-54Crossref PubMed Scopus (1065) Google Scholar, Guasto et al., 2012Guasto J.S. Rusconi R. Stocker R. Fluid mechanics of planktonic microorganisms.Annu. Rev. Fluid Mech. 2012; 44: 373-400Crossref Scopus (331) Google Scholar, Macnab, 2003Macnab R.M. How bacteria assemble flagella.Annu. Rev. Microbiol. 2003; 57: 77-100Crossref PubMed Scopus (753) Google Scholar). Here, we provide perspective on a more general but understudied aspect of mechanics in bacterial biology, namely the effects of surfaces and flow on bacterial behavior. Outside of the oceans, most bacteria in nature exist on surfaces, rather than in the bulk liquid of their fluid environments (Costerton et al., 1995Costerton J.W. Lewandowski Z. Caldwell D.E. Korber D.R. Lappin-Scott H.M. Microbial biofilms.Annu. Rev. Microbiol. 1995; 49: 711-745Crossref PubMed Scopus (4214) Google Scholar). Bacteria are equipped to live at the liquid-solid interface via the secretion of adhesive structures such as flagella, pili, exopolysaccharides, and other matrix components (Dunne, 2002Dunne Jr., W.M. Bacterial adhesion: seen any good biofilms lately?.Clin. Microbiol. Rev. 2002; 15: 155-166Crossref PubMed Scopus (1099) Google Scholar) (Figure 1A). The mechanical environment of surface-associated bacteria is remarkably different than that of their free-floating counterparts (Figure 1B). From initial contact, a surface-attached bacterium will experience a local force that is normal to the surface, usually referred to as an adhesive force (Figure 1B). In an environment with flow, the viscosity of the surrounding fluid generates a hydrodynamic (shear) force on the cell that is tangential to the surface in the direction of the flow (Figure 1B). Surface motility may produce a friction force that is tangential to the cell wall and localized at the interface with the substrate. The principles of mechanics dictate that the forces on a stationary or steadily moving cell must balance, so that a local adhesive force toward the substrate at one point on the cell must be balanced by repulsive forces due to compression elsewhere. Surface-attached bacterial cells can multiply to form large groups that develop into organized communities termed biofilms (Hall-Stoodley et al., 2004Hall-Stoodley L. Costerton J.W. Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases.Nat. Rev. Microbiol. 2004; 2: 95-108Crossref PubMed Scopus (4823) Google Scholar). At this multicellular scale, additional mechanical effects become relevant (Stewart, 2012Stewart P.S. Mini-review: convection around biofilms.Biofouling. 2012; 28: 187-198Crossref PubMed Scopus (134) Google Scholar). Attachment of a cell to a surface induces secretion of a mixture of proteins, polysaccharides, and DNA that forms a surrounding matrix (EPS; extracellular polymeric substances) with both viscous and elastic properties (Figure 1B). These extracellular polymers bind surface-attached cells and their progeny together in biofilm communities, and the rheology of the secreted matrix likely has important implications for the growth, spatial arrangement, and resilience of the resulting multicellular structures (Berk et al., 2012Berk V. Fong J.C. Dempsey G.T. Develioglu O.N. Zhuang X. Liphardt J. Yildiz F.H. Chu S. Molecular architecture and assembly principles of Vibrio cholerae biofilms.Science. 2012; 337: 236-239Crossref PubMed Scopus (275) Google Scholar, Chew et al., 2014Chew S.C. Kundukad B. Seviour T. van der Maarel J.R. Yang L. Rice S.A. Doyle P. Kjelleberg S. Dynamic remodeling of microbial biofilms by functionally distinct exopolysaccharides.mBio. 2014; 5 (e01536-01514)Crossref PubMed Scopus (121) Google Scholar). The spatiotemporal distribution of small molecules internalized and/or released by bacterial cells residing within these communities can be strongly affected by the flow environment that the community experiences, with substantial and distinct consequences for individual and collective behaviors (Figure 1B). Here, we highlight how these mechanical effects play roles in bacterial behavior at the level of single cells and of multicellular structures. We discuss strategies that bacterial cells deploy specifically on surfaces, including enhanced adhesion under fluid flow, exploration via surface-specific motility, and control of cell shape to enhance colonization (Figures 2A–2C). At the level of multicellular structures, we discuss how the rheology of polymeric matrices affects populations growing in biofilms and how flow influences these structures (Figures 2D–2F). We also describe how fluid flow affects the transport of small molecules used in social interactions—e.g., quorum sensing, between individual bacterial cells (Figure 2G). Finally, we provide insight into the scalability of the effects of mechanics on bacteria—i.e., how phenomena at the level of single cells influence emergent collective behaviors and group fitness consequences in multicellular communities. To initiate and maintain intimate contact with solid surfaces, bacteria leverage a wide variety of adhesion strategies. Many bacteria, upon attaching to a surface, will secrete a mixture of EPS, which increases their affinity for porous, rough, and chemically heterogeneous surfaces (Flemming and Wingender, 2010Flemming H.C. Wingender J. The biofilm matrix.Nat. Rev. Microbiol. 2010; 8: 623-633Crossref PubMed Scopus (5943) Google Scholar). Bacteria also construct protein structures on their exteriors that enhance their adhesion to surfaces. For example, appendages such as pili and fimbriae aid cells in overcoming repulsive forces between the cell membrane and abiotic surfaces (Figure 1A). EPS secretion and pilus formation are active areas of investigation and have been reviewed elsewhere (Burrows, 2012Burrows L.L. Pseudomonas aeruginosa twitching motility: type IV pili in action.Annu. Rev. Microbiol. 2012; 66: 493-520Crossref PubMed Scopus (416) Google Scholar, Flemming and Wingender, 2010Flemming H.C. Wingender J. The biofilm matrix.Nat. Rev. Microbiol. 2010; 8: 623-633Crossref PubMed Scopus (5943) Google Scholar). Previous reviews have also highlighted surface-specific motility such as swarming and twitching (Harshey, 2003Harshey R.M. Bacterial motility on a surface: many ways to a common goal.Annu. Rev. Microbiol. 2003; 57: 249-273Crossref PubMed Scopus (690) Google Scholar). Here, we focus on strategies bacteria use—often employing fimbriae, pili, and EPS—to maintain attachment to surfaces or to optimize surface colonization in flow environments. The shear stress generated by flow at a solid-liquid interface can easily overcome the adhesive forces anchoring cells onto a surface, potentially detaching them from substrata (De La Fuente et al., 2007De La Fuente L. Montanes E. Meng Y. Li Y. Burr T.J. Hoch H.C. Wu M. Assessing adhesion forces of type I and type IV pili of Xylella fastidiosa bacteria by use of a microfluidic flow chamber.Appl. Environ. Microbiol. 2007; 73: 2690-2696Crossref PubMed Scopus (94) Google Scholar). In flow, a cell experiences a drag force that is well estimated as Fdrag = Aσs, where A is the area of the cell exposed to flow (approximately the product of length and width for a rod-shape bacterium) and σs is the local shear stress at the surface (Berg, 1993Berg H.C. Random Walks in Biology, Expanded Edition. Princeton University Press, 1993Google Scholar). In a microfluidic channel with rectangular cross section of height h and width w, and given flow rate Q (in m3 per second), the shear stress at the wall can be estimated by σs = 6Qμ/wh2 where μ is the fluid viscosity. Although shear stress depends highly on the geometry of the flow, it is generally larger in environments with higher flow speeds. Thus, the drag force on an attached cell typically increases with flow intensity, and the attachment strength required for a cell to resist removal by shear will depend on the flows that characterize its environmental niche (Bakker et al., 2004Bakker D.P. Postmus B.R. Busscher H.J. van der Mei H.C. Bacterial strains isolated from different niches can exhibit different patterns of adhesion to substrata.Appl. Environ. Microbiol. 2004; 70: 3758-3760Crossref PubMed Scopus (60) Google Scholar). Cell adhesion forces range from a few to hundreds of picoNewtons (pN), which is sufficient to maintain attachment in a variety of flow environments. These forces also strongly depend on chemistry (Garrett et al., 2008Garrett T.R. Bhakoo M. Zhang Z. Bacterial adhesion and biofilms on surfaces.Prog. Nat. Sci. 2008; 18: 1049-1056Crossref Scopus (737) Google Scholar) and mechanical properties of the substrate (Lichter et al., 2008Lichter J.A. Thompson M.T. Delgadillo M. Nishikawa T. Rubner M.F. Van Vliet K.J. Substrata mechanical stiffness can regulate adhesion of viable bacteria.Biomacromolecules. 2008; 9: 1571-1578Crossref PubMed Scopus (188) Google Scholar). Some bacteria, like the prosthecate Caulobacter crescentus, stand out among microbial models of shear resistance with their extremely strong surface attachment. Single C. crescentus cells construct an adhesive holdfast, which is composed of a sticky substance that localizes at the cell poles, to withstand forces as large as 1 μN, which effectively renders them irreversibly surface-attached (Tsang et al., 2006Tsang P.H. Li G. Brun Y.V. Freund L.B. Tang J.X. Adhesion of single bacterial cells in the micronewton range.Proc. Natl. Acad. Sci. USA. 2006; 103: 5764-5768Crossref PubMed Scopus (172) Google Scholar). C. crescentus cells can withstand shear stresses as high as 1 MPa (their typical surface area being on the order of 1 μm2). It is not clear why C. crescentus evolved such extreme attachment strength, given that the typical shear stress in their natural freshwater environments is expected to be orders of magnitude lower. One hypothesis is that such strong attachment prevents grazing by predators (Parry, 2004Parry J.D. Protozoan grazing of freshwater biofilms.Adv. Appl. Microbiol. 2004; 54: 167-196Crossref PubMed Scopus (129) Google Scholar). Paradoxically, multiple examples exist in which increasing shear stress enhances cell attachment to surfaces. For example, Escherichia coli is subject to flows spanning a wide range of intensities as it colonizes different host tissues (Thomas et al., 2004Thomas W.E. Nilsson L.M. Forero M. Sokurenko E.V. Vogel V. Shear-dependent ‘stick-and-roll’ adhesion of type 1 fimbriated Escherichia coli.Mol. Microbiol. 2004; 53: 1545-1557Crossref PubMed Scopus (207) Google Scholar), and it has evolved adaptable fimbriae that counteract removal by flow to optimize colonization in these diverse environments (Thomas, 2008Thomas W. Catch bonds in adhesion.Annu. Rev. Biomed. Eng. 2008; 10: 39-57Crossref PubMed Scopus (149) Google Scholar). Typical bacterial fimbriae fail to maintain adherence upon application of a sufficiently large force, whereas among many strains of E. coli, type I fimbriae attachment is enhanced under increasing tensile load (Thomas et al., 2008Thomas W.E. Vogel V. Sokurenko E. Biophysics of catch bonds.Annu. Rev. Biophys. 2008; 37: 399-416Crossref PubMed Scopus (236) Google Scholar) (Figure 3A). In these cases, type I fimbriae are capped with a tip protein called FimH that specifically binds the mannose that coats the surfaces of many tissues. Under tension, the mannose-bound FimH changes conformation, adopting a strong attachment state (Le Trong et al., 2010Le Trong I. Aprikian P. Kidd B.A. Forero-Shelton M. Tchesnokova V. Rajagopal P. Rodriguez V. Interlandi G. Klevit R. Vogel V. et al.Structural basis for mechanical force regulation of the adhesin FimH via finger trap-like beta sheet twisting.Cell. 2010; 141: 645-655Abstract Full Text Full Text PDF PubMed Scopus (210) Google Scholar) (Figure 3A). This force-dependent attachment is known as a catch bond, which increases the reliability of cell attachment to the surface in strong flow environments but also leads to a “stick and roll” adhesion where cells slowly move in the direction of the flow while remaining attached to the surface (Thomas et al., 2004Thomas W.E. Nilsson L.M. Forero M. Sokurenko E.V. Vogel V. Shear-dependent ‘stick-and-roll’ adhesion of type 1 fimbriated Escherichia coli.Mol. Microbiol. 2004; 53: 1545-1557Crossref PubMed Scopus (207) Google Scholar). Catch bonds thus may be beneficial during gastrointestinal colonization, allowing cells to remain in a beneficial microenvironment by anchoring to the epithelium and modulating their shear resistance in response to flow conditions. Notably, uropathogenic strains of E. coli possess mutations in FimH that reduce the dependence of adhesion on shear stress, indicating that the benefit of a catch bond may be lost in a low-frequency pulsatile flow environment (Thomas et al., 2004Thomas W.E. Nilsson L.M. Forero M. Sokurenko E.V. Vogel V. Shear-dependent ‘stick-and-roll’ adhesion of type 1 fimbriated Escherichia coli.Mol. Microbiol. 2004; 53: 1545-1557Crossref PubMed Scopus (207) Google Scholar). E. coli cells can further strengthen attachment by leveraging the mechanical deformation of type I fimbriae. These fibers extend under tension forces, so that the force applied to a single attached cell is distributed among multiple fimbriae, decreasing the load experienced by each fiber and improving the ability of a cell to remain attached to a surface (Whitfield et al., 2014Whitfield M.J. Luo J.P. Thomas W.E. Yielding elastic tethers stabilize robust cell adhesion.PLoS Comput. Biol. 2014; 10: e1003971Crossref PubMed Scopus (8) Google Scholar). Shear stress also enhances the attachment properties of Pseudomonas aeruginosa, which exhibit longer residence times on surfaces when subjected to flow than under static conditions (Lecuyer et al., 2011Lecuyer S. Rusconi R. Shen Y. Forsyth A. Vlamakis H. Kolter R. Stone H.A. Shear stress increases the residence time of adhesion of Pseudomonas aeruginosa.Biophys. J. 2011; 100: 341-350Abstract Full Text Full Text PDF PubMed Scopus (112) Google Scholar). However, unlike E. coli, P. aeruginosa employs a mechanism that is independent of surface chemistry. Indeed, when subjected to shear, adhesion of P. aeruginosa increases on both glass and elastomeric substrata. The flow-dependent increase in residence time of P. aeruginosa is diminished in mutants lacking polar type I and IV pili (cupA1 and pilC), flagella (flgK), or the ability to synthesize certain EPS matrix components (pelA). Although these observations do not entirely eliminate the possibility of attachment via catch bonds, the findings suggest an alternative mechanism of shear-dependent adhesion whereby multiple adhesive structures participate to increase surface attachment. These two examples are not rare among bacteria, as shear-enhanced adhesion has been observed in a variety of other contexts. For example, other E.coli fimbral structures can form catch bonds with distinct ligands (Nilsson et al., 2006Nilsson L.M. Thomas W.E. Trintchina E. Vogel V. Sokurenko E.V. Catch bond-mediated adhesion without a shear threshold: trimannose versus monomannose interactions with the FimH adhesin of Escherichia coli.J. Biol. Chem. 2006; 281: 16656-16663Crossref PubMed Scopus (78) Google Scholar, Tchesnokova et al., 2010Tchesnokova V. McVeigh A.L. Kidd B. Yakovenko O. Thomas W.E. Sokurenko E.V. Savarino S.J. Shear-enhanced binding of intestinal colonization factor antigen I of enterotoxigenic Escherichia coli.Mol. Microbiol. 2010; 76: 489-502Crossref PubMed Scopus (35) Google Scholar), and increased shear stress promotes the adhesion of Staphylococcus epidermis cell clusters to human fibrinogen-coated surfaces (Weaver et al., 2011Weaver W.M. Dharmaraja S. Milisavljevic V. Di Carlo D. The effects of shear stress on isolated receptor-ligand interactions of Staphylococcus epidermidis and human plasma fibrinogen using molecularly patterned microfluidics.Lab Chip. 2011; 11: 883-889Crossref PubMed Scopus (18) Google Scholar) and of S. aureus to fibers of the mechanosensitive von Willebrand factor (Pappelbaum et al., 2013Pappelbaum K.I. Gorzelanny C. Grässle S. Suckau J. Laschke M.W. Bischoff M. Bauer C. Schorpp-Kistner M. Weidenmaier C. Schneppenheim R. et al.Ultralarge von Willebrand factor fibers mediate luminal Staphylococcus aureus adhesion to an intact endothelial cell layer under shear stress.Circulation. 2013; 128: 50-59Crossref PubMed Scopus (67) Google Scholar). Some bacterial surface interaction mechanisms simultaneously enable surface attachment and locomotion. Type IV pili, for example, are cell-surface structures that rapidly polymerize and depolymerize (Burrows, 2012Burrows L.L. Pseudomonas aeruginosa twitching motility: type IV pili in action.Annu. Rev. Microbiol. 2012; 66: 493-520Crossref PubMed Scopus (416) Google Scholar), and cells use them to move over surfaces via successive pilus extension, tip attachment, and retraction, which altogether is termed twitching motility (Gibiansky et al., 2010Gibiansky M.L. Conrad J.C. Jin F. Gordon V.D. Motto D.A. Mathewson M.A. Stopka W.G. Zelasko D.C. Shrout J.D. Wong G.C. Bacteria use type IV pili to walk upright and detach from surfaces.Science. 2010; 330: 197Crossref PubMed Scopus (146) Google Scholar, Mattick, 2002Mattick J.S. Type IV pili and twitching motility.Annu. Rev. Microbiol. 2002; 56: 289-314Crossref PubMed Scopus (908) Google Scholar). P. aeruginosa and numerous other bacteria use twitching motility to explore surfaces prior to forming biofilms (Zhao et al., 2013Zhao K. Tseng B.S. Beckerman B. Jin F. Gibiansky M.L. Harrison J.J. Luijten E. Parsek M.R. Wong G.C. Psl trails guide exploration and microcolony formation in Pseudomonas aeruginosa biofilms.Nature. 2013; 497: 388-391Crossref PubMed Scopus (242) Google Scholar). Pili extension and retraction also promote intimate contact between single cells and the host during infection (Comolli et al., 1999Comolli J.C. Hauser A.R. Waite L. Whitchurch C.B. Mattick J.S. Engel J.N. Pseudomonas aeruginosa gene products PilT and PilU are required for cytotoxicity in vitro and virulence in a mouse model of acute pneumonia.Infect. Immun. 1999; 67: 3625-3630PubMed Google Scholar). A striking architectural feature of type IV pili and other adhesive structures (e.g., flagella and holdfasts) is their strict localization to the poles of many rod-shaped cells. In environments with flow, a cell attached to a surface via a polar appendage will experience forces that tend to align the cell body with the vicinal flow field. In P. aeruginosa, which attaches to surfaces using its polar type IV pili, this phenomenon produces the surprising flow-driven behavior of upstream motion. Under flow, pilus-attached P. aeruginosa cells align in the direction of fluid movement with the piliated pole facing upstream. By successively retracting and extending pili, such cells migrate upstream, against the direction of the flow, despite the force oriented opposite to them generated by shear stress (Figure 3B) (Shen et al., 2012Shen Y. Siryaporn A. Lecuyer S. Gitai Z. Stone H.A. Flow directs surface-attached bacteria to twitch upstream.Biophys. J. 2012; 103: 146-151Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar). This behavior has also been observed in the plant pathogen Xyllela fastidiosa (Meng et al., 2005Meng Y. Li Y. Galvani C.D. Hao G. Turner J.N. Burr T.J. Hoch H.C. Upstream migration of Xylella fastidiosa via pilus-driven twitching motility.J. Bacteriol. 2005; 187: 5560-5567Crossref PubMed Scopus (212) Google Scholar), in E. coli harboring type I pili (Rangel et al., 2013Rangel D.E. Marín-Medina N. Castro J.E. González-Mancera A. Forero-Shelton M. Observation of bacterial type I pili extension and contraction under fluid flow.PLoS ONE. 2013; 8: e65563Crossref PubMed Scopus (20) Google Scholar), and it may be a general feature of surface-attached species possessing motorized polar pili. Bacteria possess a wide variety of cell morphologies, and each species robustly maintains a characteristic shape by precisely coordinating complex cell wall synthesis machineries (Typas et al., 2012Typas A. Banzhaf M. Gross C.A. Vollmer W. From the regulation of peptidoglycan synthesis to bacterial growth and morphology.Nat. Rev. Microbiol. 2012; 10: 123-136Crossref Scopus (830) Google Scholar). The function of cell shape is likely to depend on the typical environment of each species, but the underpinnings of this cell shape-niche relationship remain unknown in the vast majority of cases (Young, 2006Young K.D. The selective value of bacterial shape.Microbiol. Mol. Biol. Rev. 2006; 70: 660-703Crossref PubMed Scopus (651) Google Scholar). In some instances, however, there are hints about how cell shape may constitute an adaptation to specific environmental conditions. For example, the helical shape of Helicobacter pylori enhances swimming motility in hydrogels, a feature that aids cells in penetrating mucus layers during stomach infection (Sycuro et al., 2012Sycuro L.K. Wyckoff T.J. Biboy J. Born P. Pincus Z. Vollmer W. Salama N.R. Multiple peptidoglycan modification networks modulate Helicobacter pylori’s cell shape, motility, and colonization potential.PLoS Pathog. 2012; 8: e1002603Crossref PubMed Scopus (102) Google Scholar). In contrast, the curved bacterium C. crescentus harnesses its shape and the mechanics of its hydrodynamic environment to enhance surface colonization (Persat et al., 2014Persat A. Stone H.A. Gitai Z. The curved shape of Caulobacter crescentus enhances surface colonization in flow.Nat. Commun. 2014; 5: 3824Crossref PubMed Scopus (61) Google Scholar). As mentioned above, C. crescentus cells attach to surfaces via a polar holdfast. In flow, surface-attached cells orient in the direction of the flow (Figure 3C). Shear stress generates a torque on their curved cell bodies, which rotates them such that their unattached poles arc toward the substratum. Consequently, mother cells deposit newly born daughter cells onto the surface immediately downstream, which leads to the colonization of the downstream surface and the formation of a biofilm. Indeed, straight mutants of C. crescentus are less likely to have their progeny immediately attach to the surface following division, and such mutants are more frequently lost to the bulk flow (Persat et al., 2014Persat A. Stone H.A. Gitai Z. The curved shape of Caulobacter crescentus enhances surface colonization in flow.Nat. Commun. 2014; 5: 3824Crossref PubMed Scopus (61) Google Scholar). Thus C. crescentus may have evolved its curved shape to enhance surface colonization in environments with flow, indicating that bacterial morphology is potentially a result of adaptation to specific mechanical environments. As described above, bacteria adopt many phenotypes that can confer fitness advantages when cells are associated with a substrate. Transitioning from a planktonic swimming state to surface attachment is presumably an expensive regulatory decision in terms of energetic and potential opportunity cost. In several notable cases, bacteria coordinate transitions between attachment to and detachment from surfaces, making specific use of mechanical cues transduced via cell-surface structures. Swimming motility allows cells to explore the bulk of a fluid but becomes largely unnecessary after surface attachment. Consequently, many flagellar systems possess a mechanism for disabling rotation in response to mechanical forces. In a low Reynolds flow number environment, an object moving very close to a boundary experiences a larger viscous force compared to that which it would experience far away from the surface (Goldman et al., 1967Goldman A.J. Cox R.G. Brenner H. Slow Viscous motion of a sphere parallel to a plane wall. i. motion through a quiescent fluid.Chem. Eng. Sci. 1967; 22: 637Crossref Scopus (1129) Google Scholar). Relative to that of a planktonic cell, the rotating flagellum of a surface-attached cell experiences a significantly larger drag force, increasing the load on the flagellar motors. E. coli harnesses this hydrodynamic effect and subsequently alters flagellar rotation (Lele et al., 2013Lele P.P. Hosu B.G. Berg H.C. Dynamics of mechanosensing in the bacterial flagellar motor.Proc. Natl. Acad. Sci. USA. 2013; 110: 11839-11844Crossref PubMed Scopus (203) Google Scholar). More generally, many bacterial species exhibit behavioral changes upon inhibition of flagellar rotation. EPS secretion, for example, is strongly modulated in response to the load on flagella by B. subtilis and V. parahaemolyticus (Belas, 2014Belas R. Biofilms, flagella, and mechanosensing of surfaces by bacteria.Trends
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