Fermentation Practices Select for Thermostable Endolysins in Phages

Oechslin, Frank; Zhu, Xiaojun; Morency, Carlee; Somerville, Vincent; Shi, Rong; Moineau, Sylvain

doi:10.1093/molbev/msae055

Title: Fermentation Practices Select for Thermostable Endolysins in Phages

Journal Article · 15 March 2024 · Molecular Biology and Evolution

DOI: https://doi.org/10.1093/molbev/msae055 · OSTI ID:2470125

^[1]; Zhu, Xiaojun ^[1]; Morency, Carlee ^[1]; Somerville, Vincent ^[2]; Shi, Rong ^[1];

^[1]

Université Laval, Québec City (Canada)
Université Laval, Québec City (Canada); McGill University, Montreal, QC (Canada)

Endolysins are produced by (bacterio)phages and play a crucial role in degrading the bacterial cell wall and the subsequent release of new phage progeny. These lytic enzymes exhibit a remarkable diversity, often occurring in a multimodular form that combines different catalytic and cell wall-binding domains, even in phages infecting the same species. Yet, our current understanding lacks insight into how environmental factors and ecological niches may have influenced the evolution of these enzymes. In this study, we focused on phages infecting Streptococcus thermophilus, as this bacterial species has a well-defined and narrow ecological niche, namely, dairy fermentation. Among the endolysins found in phages targeting this species, we observed limited diversity, with a singular structural type dominating in most of identified S. thermophilus phages. Within this prevailing endolysin type, we discovered a novel and highly conserved calcium-binding motif. This motif proved to be crucial for the stability and activity of the enzyme at elevated temperatures. Ultimately, we demonstrated its positive selection within the host's environmental conditions, particularly under the temperature profiles encountered in the production of yogurt, mozzarella, and hard cheeses that rely on S. thermophilus.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); Swiss National Science Foundation

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 2470125

Journal Information:: Molecular Biology and Evolution, Journal Name: Molecular Biology and Evolution Journal Issue: 3 Vol. 41; ISSN 0737-4038

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (64)

Solution structure of the recombinant target recognition domain of zoocin A Chen, Yinghua; Simmonds, Robin S.; Young, John K. Proteins: Structure, Function, and Bioinformatics, Vol. 81, Issue 4 https://doi.org/10.1002/prot.24224	journal	January 2013
The effect of calciums on molecular motions of proteinase K Liu, Shu-Qun; Tao, Yan; Meng, Zhao-Hui Journal of Molecular Modeling, Vol. 17, Issue 2 https://doi.org/10.1007/s00894-010-0724-6	journal	May 2010
Gene cloning and expression in lactic streptococci De Vos, W. FEMS Microbiology Letters, Vol. 46, Issue 3 https://doi.org/10.1016/0378-1097(87)90113-3	journal	September 1987
Crystal structure of calcium-free proteinase K at 1.5-A resolution. Müller, A.; Hinrichs, W.; Wolf, W. M. Journal of Biological Chemistry, Vol. 269, Issue 37 https://doi.org/10.1016/S0021-9258(17)31626-5	journal	September 1994
Amidase domains from bacterial and phage autolysins define a family of γ-d,l-glutamate-specific amidohydrolases Rigden, Daniel J.; Jedrzejas, Mark J.; Galperin, Michael Y. Trends in Biochemical Sciences, Vol. 28, Issue 5 https://doi.org/10.1016/S0968-0004(03)00062-8	journal	May 2003
New insights in the molecular biology and physiology of revealed by comparative genomics Hols, P.; Hancy, F.; Fontaine, L. FEMS Microbiology Reviews, Vol. 29, Issue 3 https://doi.org/10.1016/j.femsre.2005.04.008	journal	August 2005
Safety assessment of dairy microorganisms: Streptococcus thermophilus☆ Delorme, C. International Journal of Food Microbiology, Vol. 126, Issue 3 https://doi.org/10.1016/j.ijfoodmicro.2007.08.014	journal	September 2008
Study of Streptococcus thermophilus population on a world-wide and historical collection by a new MLST scheme Delorme, Christine; Legravet, Nicolas; Jamet, Emmanuel International Journal of Food Microbiology, Vol. 242 https://doi.org/10.1016/j.ijfoodmicro.2016.11.016	journal	February 2017
A systems analysis of pasta filata process during Mozzarella cheese making Yu, Chenxu; Gunasekaran, Sundaram Journal of Food Engineering, Vol. 69, Issue 4 https://doi.org/10.1016/j.jfoodeng.2004.08.031	journal	August 2005
The viriosphere, diversity, and genetic exchange within phage communities Hambly, Emma; Suttle, Curtis A. Current Opinion in Microbiology, Vol. 8, Issue 4, p. 444-450 https://doi.org/10.1016/j.mib.2005.06.005	journal	August 2005
Bacteriophage lysins as effective antibacterials Fischetti, Vincent A. Current Opinion in Microbiology, Vol. 11, Issue 5 https://doi.org/10.1016/j.mib.2008.09.012	journal	October 2008
Structural Basis for Selective Recognition of Pneumococcal Cell Wall by Modular Endolysin from Phage Cp-1 Hermoso, Juan A.; Monterroso, Begoña; Albert, Armando Structure, Vol. 11, Issue 10 https://doi.org/10.1016/j.str.2003.09.005	journal	October 2003
Global gene expression analysis of two Streptococcus thermophilus bacteriophages using DNA microarray Duplessis, Martin; Russell, W. Michael; Romero, Dennis A. Virology, Vol. 340, Issue 2 https://doi.org/10.1016/j.virol.2005.05.033	journal	September 2005
Long-range structural changes in proteinase K triggered by calcium ion removal Bajorath, Jürgen; Raghunathan, Srinivasan; Hinrichs, Winfried Nature, Vol. 337, Issue 6206 https://doi.org/10.1038/337481a0	journal	February 1989
Dynamic personalities of proteins Henzler-Wildman, Katherine; Kern, Dorothee Nature, Vol. 450, Issue 7172 https://doi.org/10.1038/nature06522	journal	December 2007
Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus Bolotin, Alexander; Quinquis, Benoît; Renault, Pierre Nature Biotechnology, Vol. 22, Issue 12 https://doi.org/10.1038/nbt1034	journal	November 2004
Enzymatic assembly of DNA molecules up to several hundred kilobases Gibson, Daniel G.; Young, Lei; Chuang, Ray-Yuan Nature Methods, Vol. 6, Issue 5, p. 343-345 https://doi.org/10.1038/nmeth.1318	journal	April 2009
Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7 Langer, Gerrit; Cohen, Serge X.; Lamzin, Victor S. Nature Protocols, Vol. 3, Issue 7 https://doi.org/10.1038/nprot.2008.91	journal	June 2008
Detecting natural adaptation of the Streptococcus thermophilus CRISPR-Cas systems in research and classroom settings Hynes, Alexander P.; Lemay, Marie-Laurence; Trudel, Luc Nature Protocols, Vol. 12, Issue 3 https://doi.org/10.1038/nprot.2016.186	journal	February 2017
Calcium stabilizes the strongest protein fold Milles, Lukas F.; Unterauer, Eduard M.; Nicolaus, Thomas Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07145-6	journal	November 2018
Phage diversity, genomics and phylogeny Dion, Moïra B.; Oechslin, Frank; Moineau, Sylvain Nature Reviews Microbiology, Vol. 18, Issue 3 https://doi.org/10.1038/s41579-019-0311-5	journal	February 2020
ColabFold: making protein folding accessible to all Mirdita, Milot; Schütze, Konstantin; Moriwaki, Yoshitaka Nature Methods, Vol. 19, Issue 6 https://doi.org/10.1038/s41592-022-01488-1	journal	May 2022
C-terminal domains of Listeria monocytogenes bacteriophage murein hydrolases determine specific recognition and high-affinity binding to bacterial cell wall carbohydrates: Cell wall binding domains of Listeria phage lysins Loessner, Martin J.; Kramer, Karl; Ebel, Frank Molecular Microbiology, Vol. 44, Issue 2 https://doi.org/10.1046/j.1365-2958.2002.02889.x	journal	April 2002
Ray: Simultaneous Assembly of Reads from a Mix of High-Throughput Sequencing Technologies Boisvert, Sébastien; Laviolette, François; Corbeil, Jacques Journal of Computational Biology, Vol. 17, Issue 11 https://doi.org/10.1089/cmb.2009.0238	journal	November 2010
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry Journal of Computational Biology, Vol. 19, Issue 5 https://doi.org/10.1089/cmb.2012.0021	journal	May 2012
Fast and accurate short read alignment with Burrows-Wheeler transform Li, H.; Durbin, R. Bioinformatics, Vol. 25, Issue 14 https://doi.org/10.1093/bioinformatics/btp324	journal	May 2009
CD-HIT: accelerated for clustering the next-generation sequencing data Fu, Limin; Niu, Beifang; Zhu, Zhengwei Bioinformatics, Vol. 28, Issue 23 https://doi.org/10.1093/bioinformatics/bts565	journal	October 2012
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 49, Issue W1 https://doi.org/10.1093/nar/gkab301	journal	April 2021
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
The HHpred interactive server for protein homology detection and structure prediction Soding, J.; Biegert, A.; Lupas, A. N. Nucleic Acids Research, Vol. 33, Issue Web Server https://doi.org/10.1093/nar/gki408	journal	July 2005
SNPeffect 4.0: on-line prediction of molecular and structural effects of protein-coding variants De Baets, G.; Van Durme, J.; Reumers, J. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr996	journal	November 2011
Elevation of Lactococcus lactis subsp. cremoris to the species level as Lactococcus cremoris sp. nov. and transfer of Lactococcus lactis subsp. tructae to Lactococcus cremoris as Lactococcus cremoris subsp. tructae comb. nov. Li, Ting Ting; Tian, Wen Li; Gu, Chun Tao International Journal of Systematic and Evolutionary Microbiology, Vol. 71, Issue 3 https://doi.org/10.1099/ijsem.0.004727	journal	June 2019
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
PROCHECK: a program to check the stereochemical quality of protein structures Laskowski, R. A.; MacArthur, M. W.; Moss, D. S. Journal of Applied Crystallography, Vol. 26, Issue 2 https://doi.org/10.1107/S0021889892009944	journal	April 1993
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Refinement of Macromolecular Structures by the Maximum-Likelihood Method Murshudov, G. N.; Vagin, A. A.; Dodson, E. J. Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3 https://doi.org/10.1107/S0907444996012255	journal	May 1997
CheckMyMetal : a macromolecular metal-binding validation tool Zheng, Heping; Cooper, David R.; Porebski, Przemyslaw J. Acta Crystallographica Section D Structural Biology, Vol. 73, Issue 3 https://doi.org/10.1107/S2059798317001061	journal	February 2017
The measurement and significance of ionic calcium in milk – A review Lewis, Michael J. International Journal of Dairy Technology, Vol. 64, Issue 1 https://doi.org/10.1111/j.1471-0307.2010.00639.x	journal	October 2010
Peptidoglycan structure and architecture Vollmer, Waldemar; Blanot, Didier; De Pedro, Miguel A. FEMS Microbiology Reviews, Vol. 32, Issue 2 https://doi.org/10.1111/j.1574-6976.2007.00094.x	journal	March 2008
Recognition Dynamics Up to Microseconds Revealed from an RDC-Derived Ubiquitin Ensemble in Solution Lange, O. F.; Lakomek, N. -A.; Fares, C. Science, Vol. 320, Issue 5882 https://doi.org/10.1126/science.1157092	journal	June 2008
Accurate prediction of protein structures and interactions using a three-track neural network Baek, Minkyung; DiMaio, Frank; Anishchenko, Ivan Science, Vol. 373, Issue 6557 https://doi.org/10.1126/science.abj8754	journal	July 2021
Novel Genus of Phages Infecting Streptococcus thermophilus: Genomic and Morphological Characterization Philippe, Cécile; Levesque, Sébastien; Dion, Moïra B. Applied and Environmental Microbiology, Vol. 86, Issue 13 https://doi.org/10.1128/AEM.00227-20	journal	June 2020
Sequence-Function Relationships in Phage-Encoded Bacterial Cell Wall Lytic Enzymes and Their Implications for Phage-Derived Product Design Vázquez, Roberto; García, Ernesto; García, Pedro Journal of Virology, Vol. 95, Issue 14 https://doi.org/10.1128/JVI.00321-21	journal	June 2021
Molecular Aspects and Comparative Genomics of Bacteriophage Endolysins Oliveira, H.; Melo, L. D. R.; Santos, S. B. Journal of Virology, Vol. 87, Issue 8 https://doi.org/10.1128/JVI.03277-12	journal	February 2013
Widespread Distribution of a Group I Intron and Its Three Deletion Derivatives in the Lysin Gene of Streptococcus thermophilus Bacteriophages Foley, Sophie; Bruttin, Anne; Brüssow, Harald Journal of Virology, Vol. 74, Issue 2 https://doi.org/10.1128/JVI.74.2.611-618.2000	journal	January 2000
Evolution of a Lytic Bacteriophage via DNA Acquisition from the Lactococcus lactis Chromosome Moineau, Sylvain; Pandian, Sithian; Klaenhammer, Todd R. Applied and Environmental Microbiology, Vol. 60, Issue 6 https://doi.org/10.1128/aem.60.6.1832-1841.1994	journal	June 1994
Holins: The Protein Clocks of Bacteriophage Infections Wang, Ing-Nang; Smith, David L.; Young, Ry Annual Review of Microbiology, Vol. 54, Issue 1 https://doi.org/10.1146/annurev.micro.54.1.799	journal	October 2000
Bacteriophages of lactic acid bacteria and their impact on milk fermentations Garneau, Josiane E.; Moineau, Sylvain Microbial Cell Factories, Vol. 10, Issue Suppl 1 https://doi.org/10.1186/1475-2859-10-S1-S20	journal	January 2011
Phage endolysins are adapted to specific hosts and are evolutionarily dynamic Oechslin, Frank; Zhu, Xiaojun; Dion, Moira B. PLOS Biology, Vol. 20, Issue 8 https://doi.org/10.1371/journal.pbio.3001740	journal	August 2022
Genes but Not Genomes Reveal Bacterial Domestication of Lactococcus Lactis Passerini, Delphine; Beltramo, Charlotte; Coddeville, Michele PLoS ONE, Vol. 5, Issue 12 https://doi.org/10.1371/journal.pone.0015306	journal	December 2010
Structural and functional insights into a novel two-component endolysin encoded by a single gene in Enterococcus faecalis phage Zhou, Biao; Zhen, Xiangkai; Zhou, Huan PLOS Pathogens, Vol. 16, Issue 3 https://doi.org/10.1371/journal.ppat.1008394	journal	March 2020
Bacteriophage endolysins as novel antimicrobials Schmelcher, Mathias; Donovan, David M.; Loessner, Martin J. Future Microbiology, Vol. 7, Issue 10 https://doi.org/10.2217/fmb.12.97	journal	October 2012
Structure and Physical Properties of Yogurt Gels: Effect of Inoculation Rate and Incubation Temperature Lee, W. J.; Lucey, J. A. Journal of Dairy Science, Vol. 87, Issue 10 https://doi.org/10.3168/jds.S0022-0302(04)73450-5	journal	October 2004
Thousands of Novel Endolysins Discovered in Uncultured Phage Genomes Fernández-Ruiz, Iris; Coutinho, Felipe H.; Rodriguez-Valera, Francisco Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01033	journal	May 2018
Enzymes and Mechanisms Employed by Tailed Bacteriophages to Breach the Bacterial Cell Barriers Fernandes, Sofia; São-José, Carlos Viruses, Vol. 10, Issue 8 https://doi.org/10.3390/v10080396	journal	July 2018
Phages in nature Clokie, Martha R. J.; Millard, Andrew D.; Letarov, Andrey V. Bacteriophage, Vol. 1, Issue 1 https://doi.org/10.4161/bact.1.1.14942	journal	January 2011
Bacteriophages and dairy fermentations Marcó, Mariángeles Briggiler; Moineau, Sylvain; Quiberoni, Andrea Bacteriophage, Vol. 2, Issue 3 https://doi.org/10.4161/bact.21868	journal	July 2012
Phage therapy: An alternative to antibiotics in the age of multi-drug resistance Lin, Derek M.; Koskella, Britt; Lin, Henry C. World Journal of Gastrointestinal Pharmacology and Therapeutics, Vol. 8, Issue 3 https://doi.org/10.4292/wjgpt.v8.i3.162	journal	January 2017
Haplotype-based variant detection from short-read sequencing Garrison, Erik; Marth, Gabor arXiv https://doi.org/10.48550/arXiv.1207.3907	preprint	January 2012
Enterococcus faecium secreted antigen A generates muropeptides to enhance host immunity and limit bacterial pathogenesis Kim, Byungchul; Wang, Yen-Chih; Hespen, Charles W. eLife, Vol. 8 https://doi.org/10.7554/eLife.45343	journal	April 2019

Similar Records

Characterization of Lactobacilli Phage Endolysins and Their Functional Domains–Potential Live Biotherapeutic Testing Reagents

Journal Article · 2023 · Viruses · OSTI ID:2471366

Dorosky, Robert J.; Lola, Stephanie L.; Brown, Haleigh A.; +3 more

Phages of lactic acid bacteria: The role of genetics in understanding phage-host interactions and their co-evolutionary processes

Journal Article · 2012 · Virology · OSTI ID:22150085

Mahony, Jennifer; Ainsworth, Stuart; Stockdale, Stephen

Toward Understanding Phage:Host Interactions in the Rumen; Complete Genome Sequences of Lytic Phages Infecting Rumen Bacteria

Journal Article · 2017 · Frontiers in Microbiology · OSTI ID:1524080

Gilbert, Rosalind A.; Kelly, William J.; Altermann, Eric; +4 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Streptococcus thermophilus
bacteriophages
biochemistry & molecular biology
dairy fermentation
endolysins
evolutionary biology
experimental evolution
genetics & heredity
host adaptation

Title: Fermentation Practices Select for Thermostable Endolysins in Phages

Citation Formats

References (64)

Similar Records

Related Subjects