Pantoea stewartii WceF is a glycan biofilm-modifying enzyme with a bacteriophage tailspike-like fold

Abstract

Pathogenic microorganisms often reside in glycan-based biofilms. Concentration and chain length distribution of these mostly anionic exopolysaccharides (EPS) determine the overall biophysical properties of a biofilm and result in a highly viscous environment. Bacterial communities regulate this biofilm state via intracellular small-molecule signaling to initiate EPS synthesis. Reorganization or degradation of this glycan matrix, however, requires the action of extracellular glycosidases. So far, these were mainly described for bacteriophages that must degrade biofilms for gaining access to host bacteria. The plant pathogen Pantoea stewartii (P. stewartii) encodes the protein WceF within its EPS synthesis cluster. WceF has homologs in various biofilm forming plant pathogens of the Erwinia family. In this work, we show that WceF is a glycosidase active on stewartan, the main P. stewartii EPS biofilm component. WceF has remarkable structural similarity with bacteriophage tailspike proteins (TSPs). Crystal structure analysis showed a native trimer of right-handed parallel β-helices. Despite its similar fold, WceF lacks the high stability found in bacteriophage TSPs. WceF is a stewartan hydrolase and produces oligosaccharides, corresponding to single stewartan repeat units. However, compared with a stewartan-specific glycan hydrolase of bacteriophage origin, WceF showed lectin-like autoagglutination with stewartan, resulting in notably slower EPS cleavage velocities. This emphasizes that the bacterial enzyme WceF has a role in P. stewartii biofilm glycan matrix reorganization clearly different from that of a bacteriophage exopolysaccharide depolymerase. Pathogenic microorganisms often reside in glycan-based biofilms. Concentration and chain length distribution of these mostly anionic exopolysaccharides (EPS) determine the overall biophysical properties of a biofilm and result in a highly viscous environment. Bacterial communities regulate this biofilm state via intracellular small-molecule signaling to initiate EPS synthesis. Reorganization or degradation of this glycan matrix, however, requires the action of extracellular glycosidases. So far, these were mainly described for bacteriophages that must degrade biofilms for gaining access to host bacteria. The plant pathogen Pantoea stewartii (P. stewartii) encodes the protein WceF within its EPS synthesis cluster. WceF has homologs in various biofilm forming plant pathogens of the Erwinia family. In this work, we show that WceF is a glycosidase active on stewartan, the main P. stewartii EPS biofilm component. WceF has remarkable structural similarity with bacteriophage tailspike proteins (TSPs). Crystal structure analysis showed a native trimer of right-handed parallel β-helices. Despite its similar fold, WceF lacks the high stability found in bacteriophage TSPs. WceF is a stewartan hydrolase and produces oligosaccharides, corresponding to single stewartan repeat units. However, compared with a stewartan-specific glycan hydrolase of bacteriophage origin, WceF showed lectin-like autoagglutination with stewartan, resulting in notably slower EPS cleavage velocities. This emphasizes that the bacterial enzyme WceF has a role in P. stewartii biofilm glycan matrix reorganization clearly different from that of a bacteriophage exopolysaccharide depolymerase. Many microorganisms produce extracellular matrices composed of polymeric substances to organize themselves in microbial communities (1Flemming H.C. Wingender J. Szewzyk U. Steinberg P. Rice S.A. Kjelleberg S. Biofilms: An emergent form of bacterial life.Nat. Rev. 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In turn, changing these macromolecular structures offers an additional control level in biofilms, for example, by matrix-degrading enzymes. For glycan-based biofilm components, regulatory glycosidases have been frequently described, in both bacterial and fungal species that can have impact on biofilm synthesis and export (7Bamford N.C. Le Mauff F. Subramanian A.S. Yip P. Millan C. Zhang Y.Z. Zacharias C. Forman A. Nitz M. Codee J.D.C. Uson I. Sheppard D.C. Howell P.L. Ega3 from the fungal pathogen Aspergillus fumigatus is an endo-alpha-1,4-galactosaminidase that disrupts microbial biofilms.J. Biol. Chem. 2019; 294: 13833-13849Abstract Full Text Full Text PDF PubMed Scopus (17) Google Scholar, 8Baker P. Whitfield G.B. Hill P.J. Little D.J. Pestrak M.J. Robinson H. Wozniak D.J. Howell P.L. Characterization of the Pseudomonas aeruginosa glycoside hydrolase PsIG reveals that its levels are critical for psi polysaccharide biosynthesis and biofilm formation.J. Biol. 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These polysaccharide-specific enzymes can alter biofilm viscosity and thus influence the mobility of biofilm-matrix embedded or penetrating particles such as bacteria or bacteriophages, making them promising tools in antimicrobial treatments (12Snarr B.D. Baker P. Bamford N.C. Sato Y. Liu H. Lehoux M. Gravelat F.N. Ostapska H. Baistrocchi S.R. Cerone R.P. Filler E.E. Parsek M.R. Filler S.G. Howell P.L. Sheppard D.C. Microbial glycoside hydrolases as antibiofilm agents with cross-kingdom activity.Proc. Natl. Acad. Sci. U. S. A. 2017; 114: 7124-7129Crossref PubMed Scopus (50) Google Scholar, 13Pestrak M.J. Baker P. Dellos-Nolan S. Hill P.J. da Silva D.P. Silver H. Lacdao I. Raju D. Parsek M.R. Wozniak D.J. Howell P.L. Treatment with the Pseudomonas aeruginosa glycoside hydrolase PslG combats wound infection by improving antibiotic efficacy and host innate immune activity.Antimicrob. Agents Chemother. 2019; 63e00234-19Crossref PubMed Scopus (31) Google Scholar, 14Dunsing V. Irmscher T. 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Plant Pathol. 2011; 12: 628-637Crossref PubMed Scopus (67) Google Scholar). P. stewartii infects sweet corn and maize where it colonizes the xylem with dense biofilms containing the exopolysaccharide stewartan as key virulence factor. Consequently, free water flow in the plants is blocked, ultimately leading to wilting of leaves and necrosis of crops. Stewartan is an anionic heteropolymer of heptasaccharide repeat structure is with M. A. V. T. Zhang K. of stewartan, the capsular exopolysaccharide from the corn pathogen Erwinia PubMed Scopus Google Scholar, A. L. and of three stewartan exopolysaccharide in Pantoea stewartii Microbiol. PubMed Scopus Google Scholar). of is by Biofilm formation in P. stewartii is by quorum sensing that three A. L. and of three stewartan exopolysaccharide in Pantoea stewartii Microbiol. PubMed Scopus Google Scholar). stewartan are on the that encodes for a exopolysaccharide synthesis A. L. and of three stewartan exopolysaccharide in Pantoea stewartii Microbiol. PubMed Scopus Google Scholar, Whitfield C. Rev. PubMed Scopus Google Scholar). by stewartan However, the additional and found to a is not required for P. stewartii The as is highly in Pantoea and Erwinia species and encodes an chain a for the corresponding protein WceF has not been in in an stewartan exopolysaccharide of to and a role of WceF in stewartan chain length control M. C. A. K. in the of the capsular exopolysaccharides and J. Biol. PubMed Scopus Google Scholar). In this work, we the structure of WceF and its with stewartan WceF high structural similarity to bacteriophage tailspike proteins and is active on stewartan, a role in exopolysaccharide modification P. stewartii is in the biofilm and WceF the of the that encodes for export via the for proteins K. of protein by the Biol. Chem. 2015; 290: Full Text Full Text PDF PubMed Scopus Google Scholar). are by a the protein has been that the native form of its structure to a for WceF to were in the As by WceF is a native of chain is composed of an a the right-handed parallel by a a and a The is of containing by three not for the the of The of WceF is formed by a of by an the of the the chain a and that form of a in the native trimer The and form a with a composed of in the of three and are by a the highly in the native trimer The WceF is in the as due to its to the of the of bacteriophage S. S. U. A. R. R. tailspike Crystal structure of the structure of the and the of and Biol. PubMed Scopus Google Scholar, A. Y. He C.J. F. M. F. of proteins via 2017; PubMed Scopus Google Scholar). structural with the high similarity of the WceF to the L. P. in PubMed Scopus Google Scholar). The WceF the WceF and the with a similar the in of bacteriophage M. A.S. S. S.A. M. L. and of the complex of bacteriophage Biol. 2019; PubMed Scopus Google Scholar). An analysis various structural homologs of WceF L. A. D. J. M. F. J. V. with a its Biol. 2018; PubMed Scopus Google Scholar). As three we from and M. A.S. S. S.A. M. L. and of the complex of bacteriophage Biol. 2019; PubMed Scopus Google Scholar, H. D. M. D. S. bacteriophage PubMed Scopus Google Scholar, J. H. Y. D.C. and tailspike glycosidase of from 2019; PubMed Scopus Google Scholar, A. D. U. R. of the protein and of the Biol. 2014; PubMed Scopus Google Scholar). were bacteriophage containing of right-handed similar to WceF structural with a of anionic polysaccharide mainly were for the WceF are enzymes to bacteriophage extracellular S. M. A. R. tailspike proteins with as PubMed Scopus Google Scholar). native are resulting in in the of In and in of its of similar to the found in WceF in the of WceF as a in the of bacteriophages and native in the of As only into to for to S. R. tailspike of effects of on Sci. PubMed Scopus Google Scholar). the bacterial protein WceF is notably in the of compared with the of bacteriophage This is in with a overall WceF trimer For and similar trimer were however, due to their different surface the WceF trimer to compared with the produced WceF to their influence on trimer only the were but were in trimer the or the the were This is in to where the for trimer M. A. S. R. and of tailspike the J. PubMed Scopus Google we that is a native trimer only in the of its activity on polysaccharide exopolysaccharide biofilms, or is found in bacteriophage where it can the infection A. Y. enzymes to the barriers the infection Microbiol. 2017; PubMed Scopus Google Scholar, Y. A. D. J. U. Barbirz S. from an bacteriophage with a Biol. Chem. 2019; 294: Full Text Full Text PDF PubMed Scopus (12) Google Scholar). parallel of have been often found to in glycan P. L. M. J. of parallel from reveals an with microbial Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar). WceF interactions with stewartan as the P. stewartii biofilm exopolysaccharide component. Stewartan from P. stewartii biofilms is highly viscous in V. Irmscher T. Barbirz S. Chiantia S. Purely polysaccharide-based biofilm matrix provides size-selective diffusion barriers for nanoparticles and bacteriophages.Biomacromolecules. 2019; 20: 3842-3854Crossref PubMed Scopus (15) Google Scholar). However, with stewartan their viscosity From we stewartan cleavage and for formation were produced a of with the Zhang J. Zhang Zhang of activity of as a 2011; Scopus Google Scholar). However, this we a in formation WceF or stewartan not produce the of the WceF showed activity that with found the as it for formation due to a polysaccharide lyase thus that WceF is a glycoside hydrolase specific for P. stewartii is host for a of WceF with a bacteriophage we the tailspike depolymerase from with WceF of a bacteriophage polysaccharide depolymerase and its in Erwinia Plant Google Scholar). stewartan the enzymatic formation of from stewartan within active a and and of the we to a enzyme compared with the with WceF to to the of the enzymatic The bacteriophage depolymerase notably the bacterial enzyme As described we to produce stewartan of and repeat M. A. T. V. Zhang F. D. K. of the capsular exopolysaccharide from the pathogen Erwinia PubMed Scopus Google Scholar). the of in stewartan these as in to stewartan cleavage by WceF or to the different cleavage found for both we compared different for WceF and for From the similar compared with the stewartan we that WceF stewartan to In the mainly produced and analysis that WceF produced of stewartan that is a stewartan a diffusion for nanoparticles V. Irmscher T. Barbirz S. Chiantia S. Purely polysaccharide-based biofilm matrix provides size-selective diffusion barriers for nanoparticles and bacteriophages.Biomacromolecules. 2019; 20: 3842-3854Crossref PubMed Scopus (15) Google Scholar). of WceF are proteins that only in viscous stewartan As WceF a of formation we the diffusion of an WceF with found that in the of stewartan, WceF to as by the of However, WceF with stewartan, we with an of to that WceF into protein of this are to in stewartan V. Irmscher T. Barbirz S. Chiantia S. Purely polysaccharide-based biofilm matrix provides size-selective diffusion barriers for nanoparticles and bacteriophages.Biomacromolecules. 2019; 20: 3842-3854Crossref PubMed Scopus (15) Google Scholar). Stewartan were to to stewartan, however, not cleavage for the stewartan depolymerase diffusion of particles in the stewartan matrix both in the and in the of as by V. Irmscher T. Barbirz S. Chiantia S. Purely polysaccharide-based biofilm matrix provides size-selective diffusion barriers for nanoparticles and bacteriophages.Biomacromolecules. 2019; 20: 3842-3854Crossref PubMed Scopus (15) Google proteins have been described in the synthesis and export that control bacterial and fungal extracellular in or biofilm In this the of enzymes that of these proteins with to their in polysaccharide modification (7Bamford N.C. Le Mauff F. Subramanian A.S. Yip P. Millan C. Zhang Y.Z. Zacharias C. Forman A. Nitz M. Codee J.D.C. Uson I. Sheppard D.C. Howell P.L. 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Periplasmic depolymerase provides insight into ABC transporter-dependent secretion of bacterial capsular polysaccharides.Proc. Natl. Acad. Sci. U. S. A. 2018; 115: E4870-E4879Crossref PubMed Scopus (12) Google Scholar, G.B. Howell P.L. of exopolysaccharides bacterial Microbiol. 2015; PubMed Google Scholar). This showed that Pantoea stewartii as of the biofilm synthesis is a active on P. biofilm exopolysaccharide stewartan, and with a bacteriophage WceF is a native trimer of right-handed β-helices. This is in proteins from species that are in and enzymatic modification of P. L. M. J. of parallel from reveals an with microbial Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar). right-handed in such as in J. R. and of parallel Biol. PubMed Scopus (106) Google or as such as in bacteriophage D. Y. U. A. S. M. Barbirz S. by from bacteriophage Sci. 2017; Google Scholar). has been found in of a hydrolase in capsular polysaccharide modification S.D. McMahon S.A. Le Bas A. Suits M.D.L. Naismith J.H. Whitfield C. Periplasmic depolymerase provides insight into ABC transporter-dependent secretion of bacterial capsular polysaccharides.Proc. Natl. Acad. Sci. U. S. A. 2018; 115: E4870-E4879Crossref PubMed Scopus (12) Google but in biofilm or enzymes of fungal or bacterial can (7Bamford N.C. Le Mauff F. Subramanian A.S. Yip P. Millan C. Zhang Y.Z. Zacharias C. Forman A. Nitz M. Codee J.D.C. Uson I. Sheppard D.C. Howell P.L. Ega3 from the fungal pathogen Aspergillus fumigatus is an endo-alpha-1,4-galactosaminidase that disrupts microbial biofilms.J. Biol. Chem. 2019; 294: 13833-13849Abstract Full Text Full Text PDF PubMed Scopus (17) Google Scholar, D.J. R. Le Mauff F. Bamford N.C. C. Baker P. M. Robinson H. G.B. Nitz M. R. Sheppard D.C. Howell P.L. a glycoside hydrolase that and can bacterial 2018; PubMed Scopus Google Scholar, N.C. B.D. Gravelat F.N. Little D.J. M.J. Zacharias J.C. S.D. Baker P. Robinson H. Howell P.L. Sheppard D.C. is a glycoside hydrolase required for the biosynthesis of in Aspergillus Biol. Chem. 2015; 290: Full Text Full Text PDF PubMed Scopus Google Scholar). P. stewartii WceF is the enzyme of this that as a So far, these have only been found as of bacteriophage TSPs. are proteins that in glycan and cleavage to the infection in bacteriophages Y. A. D. J. U. Barbirz S. from an bacteriophage with a Biol. Chem. 2019; 294: Full Text Full Text PDF PubMed Scopus (12) Google Scholar, D. C. U. Barbirz S. R. interactions with from particles in Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar, Barbirz S. a but a bacteriophages as an essential to initiate Microbiol. 2017; PubMed Scopus Google Scholar). structures with for specific with proteins of the and that in host glycan M. A.S. S. S.A. M. L. and of the complex of bacteriophage Biol. 2019; PubMed Scopus Google Scholar, A. Y. the architecture of proteins in Microbiol. 2019; PubMed Scopus Google Scholar). not only the WceF but also its and the the are to similar in bacteriophage TSPs. is thus to that P. stewartii has WceF with bacteriophages to in modification of biofilm the have The structural of the WceF found in bacteriophage in but is for protein or trimer M. A. S. R. and of tailspike the J. PubMed Scopus Google Scholar). this is and highly However, WceF this were and we were to the role of this for WceF trimer This that WceF is not and it in the of in to the high stability for S. M. A. R. tailspike proteins with as PubMed Scopus Google Scholar). The specific WceF single chain and trimer for these stability For example, in the WceF the lacks a turn, but has a that a parallel of the resulting in a trimer compared with the different interactions alter trimer WceF has a In showed that WceF stewartan In stewartan enzymatic with the depolymerase of bacteriophage WceF a and production only WceF formed in the of From the WceF we that the of these highly dense protein to WceF that can form in a stewartan showed that stewartan as a in diffusion is by both polysaccharide chain and interactions with the matrix V. Irmscher T. Barbirz S. Chiantia S. Purely polysaccharide-based biofilm matrix provides size-selective diffusion barriers for nanoparticles and bacteriophages.Biomacromolecules. 2019; 20: 3842-3854Crossref PubMed Scopus (15) Google Scholar). that WceF by with in for and interactions P. H. F. K.E. H.C. Wingender J. extracellular and the polysaccharide alginate of Pseudomonas Microbiol. PubMed Scopus Google Scholar). The WceF trimer thus stewartan in to and Biol. Chem. Full Text Full Text PDF PubMed Scopus Google we not a of stewartan or in the of the of WceF with its for a of stewartan structural for Sci. PubMed Scopus Google Scholar). is a a high of the enzyme the and a is in with the activity for WceF to the stewartan and the chain single stewartan As a the of stewartan in a In with WceF as an of showed In stewartan is by and a of showed that diffusion of particles in the stewartan matrix in a for the to the biofilm V. Irmscher T. Barbirz S. Chiantia S. Purely polysaccharide-based biofilm matrix provides size-selective diffusion barriers for nanoparticles and bacteriophages.Biomacromolecules. 2019; 20: 3842-3854Crossref PubMed Scopus (15) Google Scholar). bacteriophage also WceF produces that to single of its glycan heteropolymer thus must S. C. U. R. Crystal structure of tailspike are Microbiol. PubMed Scopus Google Scholar). From this it that exopolysaccharide is in the where are but not to a role of WceF for extracellular glycan The of WceF homologs in Pantoea species to a role of these proteins that is not WceF a for however, in this we have not its WceF formation with stewartan, as in this work, the biofilm matrix by of particles with is a found in bacterial biofilms, in the extracellular matrix of S. or of with in biofilms L. Singh P.K. Hartmann R. Nadell C.D. Drescher K. Dynamic biofilm architecture confers individual and collective mechanisms of viral protection.Nat. Microbiol. 2018; 3: 26-31Crossref PubMed Scopus (110) Google Scholar, R. J. analysis to complex biofilm 2011; PubMed Scopus Google Scholar, M.J. of and antibiotic on biofilm PubMed Scopus Google Scholar). In these of or a similar to the WceF in this In chain length and determine a properties in for example, critical and thus its properties as a matrix J. K. The in the through 2017; PubMed Google Scholar). chain of exopolysaccharides by can to control external glycan properties P. Whitfield G.B. Hill P.J. Little D.J. Pestrak M.J. Robinson H. Wozniak D.J. Howell P.L. Characterization of the Pseudomonas aeruginosa glycoside hydrolase PsIG reveals that its levels are critical for psi polysaccharide biosynthesis and biofilm formation.J. Biol. Chem. 2015; 290: 28374-28387Abstract Full Text Full Text PDF PubMed Scopus (39) Google Scholar, 10Liston S.D. McMahon S.A. Le Bas A. Suits M.D.L. Naismith J.H. Whitfield C. Periplasmic depolymerase provides insight into ABC transporter-dependent secretion of bacterial capsular polysaccharides.Proc. Natl. Acad. Sci. U. S. A. 2018; 115: E4870-E4879Crossref PubMed Scopus (12) Google Scholar, H. The Rev. Microbiol. PubMed Scopus Google Scholar). of in the WceF stewartan biosynthesis the chain length to the by by polysaccharide interactions with its V. P.J. Whitfield C. structure of by reveals into 2017; Full Text Full Text PDF PubMed Scopus Google Scholar). P. stewartii were found to the stewartan chain M. C. A. K. in the of the capsular exopolysaccharides and J. Biol. PubMed Scopus Google Scholar). thus that WceF is active on stewartan of WceF activity in the biofilm regulate the chain length distribution to its overall V. Irmscher T. Barbirz S. Chiantia S. Purely polysaccharide-based biofilm matrix provides size-selective diffusion barriers for nanoparticles and bacteriophages.Biomacromolecules. 2019; 20: 3842-3854Crossref PubMed Scopus (15) Google Scholar). in for WceF to its different P. stewartii also and of the protein by the exopolysaccharide synthesis of P. that specific protein interactions regulate biofilm Biofilm on its as a viscous matrix that can as a and a of the determines these biophysical properties (3Moradali M.F. Rehm B.H.A. Bacterial biopolymers: From pathogenesis to advanced materials.Nat. Rev. Microbiol. 2020; 18: 195-210Crossref PubMed Scopus (112) Google Scholar). but also that are active on polymeric glycan thus in matrix glycan in biofilms by bacterial glycosidases has impact on biofilm dispersal also in K.P. Sauer K. Biofilm dispersion.Nat. Rev. Microbiol. 2020; 18: 571-586Crossref PubMed Scopus (127) Google Scholar, 11Cherny K.E. Sauer K. Untethering and degradation of the polysaccharide matrix are essential steps in the dispersion response of Pseudomonas aeruginosa biofilms.J. Bacteriol. 2020; 202e00575-19Crossref PubMed Scopus (11) Google Scholar). P. stewartii WceF as a structure for a of protein homologs in plant pathogens of that or on these also to the for of biofilm properties with for pathogen control or (1Flemming H.C. Wingender J. Szewzyk U. Steinberg P. Rice S.A. Kjelleberg S. Biofilms: An emergent form of bacterial life.Nat. Rev. Microbiol. 2016; 14: 563-575Crossref PubMed Scopus (2050) Google Scholar, D. L. 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