Lysozyme Resistance in Streptococcus suis Is Highly Variable and Multifactorial
Publication Date
April 30, 2012
Journal
PLOS ONE
Authors
Paul J. Wichgers Schreur, Christian Van Weeghel, Johanna M. J. Rebel, Mari A. Smits, et al
Volume
7
Issue
4
Pages
e36281
DOI
https://dx.plos.org/10.1371/journal.pone.0036281
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0036281
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/22558419
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3340348
Europe PMC
http://europepmc.org/abstract/MED/22558419
Web of Science
000305340200060
Scopus
84860451053
Mendeley
http://www.mendeley.com/research/lysozyme-resistance-streptococcus-suis-highly-variable-multifactorial
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Mendeley | Further Information

{"title"=>"Lysozyme resistance in streptococcus suis is highly variable and multifactorial", "type"=>"journal", "authors"=>[{"first_name"=>"Paul J.", "last_name"=>"Schreur", "scopus_author_id"=>"43361782700"}, {"first_name"=>"Christian", "last_name"=>"van Weeghel", "scopus_author_id"=>"55203583600"}, {"first_name"=>"Johanna M J", "last_name"=>"Rebel", "scopus_author_id"=>"7003863878"}, {"first_name"=>"Mari A.", "last_name"=>"Smits", "scopus_author_id"=>"7006388297"}, {"first_name"=>"Jos P M", "last_name"=>"van Putten", "scopus_author_id"=>"7005243089"}, {"first_name"=>"Hilde E.", "last_name"=>"Smith", "scopus_author_id"=>"7406226559"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "doi"=>"10.1371/journal.pone.0036281", "pui"=>"364721046", "sgr"=>"84860451053", "scopus"=>"2-s2.0-84860451053", "pmid"=>"22558419", "issn"=>"19326203"}, "id"=>"72ecdfa5-96fe-3f8f-8f67-c9b98294f54f", "abstract"=>"BACKGROUND: Streptococcus suis is an important infectious agent for pigs and occasionally for humans. The host innate immune system plays a key role in preventing and eliminating S. suis infections. One important constituent of the innate immune system is the protein lysozyme, which is present in a variety of body fluids and immune cells. Lysozyme acts as a peptidoglycan degrading enzyme causing bacterial lysis. Several pathogens have developed mechanisms to evade lysozyme-mediated killing. In the present study we compared the lysozyme sensitivity of various S. suis isolates and investigated the molecular basis of lysozyme resistance for this pathogen.\\n\\nRESULTS: The lysozyme minimal inhibitory concentrations of a wide panel of S. suis isolates varied between 0.3 to 10 mg/ml. By inactivating the oatA gene in a serotype 2 and a serotype 9 strain, we showed that OatA-mediated peptidoglycan modification partly contributes to lysozyme resistance. Furthermore, inactivation of the murMN operon provided evidence that additional peptidoglycan crosslinking is not involved in lysozyme resistance in S. suis. Besides a targeted approach, we also used an unbiased approach for identifying factors involved in lysozyme resistance. Based on whole genome comparisons of a lysozyme sensitive strain and selected lysozyme resistant derivatives, we detected several single nucleotide polymorphisms (SNPs) that were correlated with the lysozyme resistance trait. Two SNPs caused defects in protein expression of an autolysin and a capsule sugar transferase. Analysis of specific isogenic mutants, confirmed the involvement of autolysin activity and capsule structures in lysozyme resistance of S. suis.\\n\\nCONCLUSIONS: This study shows that lysozyme resistance levels are highly variable among S. suis isolates and serotypes. Furthermore, the results show that lysozyme resistance in S. suis can involve different mechanisms including OatA-mediated peptidolycan modification, autolysin activity and capsule production.", "link"=>"http://www.mendeley.com/research/lysozyme-resistance-streptococcus-suis-highly-variable-multifactorial", "reader_count"=>24, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Student > Doctoral Student"=>3, "Researcher"=>3, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Other"=>2, "Student > Master"=>4, "Student > Bachelor"=>6}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Student > Doctoral Student"=>3, "Researcher"=>3, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Other"=>2, "Student > Master"=>4, "Student > Bachelor"=>6}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>16, "Veterinary Science and Veterinary Medicine"=>1, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>16}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>3}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "United Kingdom"=>1, "Germany"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/645609"], "description"=>"<p>Growth of <i>S. suis</i> strain 10 (wild type), strain 10-LysR-1 and strain 10-LysR-2 in THB (A) and in THB supplemented with 500 µg/ml lysozyme (B). Values represent the mean of three independent experiments. At almost all time points (three per hour) SD values were maximal 30% of the indicated values.</p>", "links"=>[], "tags"=>["curves", "10-lysr-1", "10-lysr-2"], "article_id"=>316094, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Paul J. Wichgers Schreur", "Christian van Weeghel", "Johanna M. J. Rebel", "Mari A. Smits", "Jos P. M. van Putten", "Hilde E. Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036281.g004", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Growth_curves_of_wild_type_10_LysR_1_and_10_LysR_2_S_suis_strains_/316094", "title"=>"Growth curves of wild type, 10-LysR-1 and 10-LysR-2 <i>S. suis</i> strains.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-30 01:41:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/645680"], "description"=>"<p>Strain 10 (wild type), strain 10-LysR-1, 10-LysR-2, 10-Δ0475, 10-Δ<i>cps2EF</i> and 10-LysR-2-<i>cps2E</i> were spotted onto Colombia agar plates containing two-fold increasing concentrations of lysozyme. Growth was assessed 24 h later and MICs were determined. Values represent three independent observations. No error bars are displayed since the MIC values were identical in replicate experiments.</p>", "links"=>[], "tags"=>["mic", "levels", "autolysin", "capsule", "mutant"], "article_id"=>316169, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Paul J. Wichgers Schreur", "Christian van Weeghel", "Johanna M. J. Rebel", "Mari A. Smits", "Jos P. M. van Putten", "Hilde E. Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036281.g005", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lysozyme_MIC_levels_of_autolysin_and_capsule_mutant_strains_/316169", "title"=>"Lysozyme MIC levels of autolysin and capsule mutant strains.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-30 01:42:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/646046"], "description"=>"<p>Serotype 2 strains were separated into two (A and B) different genetic clusters based on CGH data <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036281#pone.0036281-deGreeff1\" target=\"_blank\">[22]</a>. The numbers between brackets represent the number of positive PCR products compared to the total number of analyzed isolates.</p>", "links"=>[], "tags"=>["genes", "encoding", "peptidoglycan", "modifying", "enzymes"], "article_id"=>316529, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Paul J. Wichgers Schreur", "Christian van Weeghel", "Johanna M. J. Rebel", "Mari A. Smits", "Jos P. M. van Putten", "Hilde E. Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036281.t001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Distribution_of_genes_encoding_peptidoglycan_modifying_enzymes_in_different_S_suis_serotypes_/316529", "title"=>"Distribution of genes encoding peptidoglycan modifying enzymes in different <i>S. suis</i> serotypes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-04-30 01:48:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/645322"], "description"=>"<p>Wild type serotype 1, 2, 7 and 9 isolates (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036281#pone.0036281.s002\" target=\"_blank\">Table S2</a>) were spotted onto Colombia agar plates containing two-fold increasing concentrations of lysozyme (start concentration: 62.5 µg/ml). Growth was assessed 24 h later and MICs were determined. Serotype 2 strains were separated into two (A and B) different genetic clusters based on CGH data <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036281#pone.0036281-deGreeff1\" target=\"_blank\">[22]</a>. Each isolate is represented by a dot and one dot represents the mean of two independent observations. The red lines represent the mean resistance level and SD of the indicated groups.</p>", "links"=>[], "tags"=>["mic", "levels"], "article_id"=>315809, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Paul J. Wichgers Schreur", "Christian van Weeghel", "Johanna M. J. Rebel", "Mari A. Smits", "Jos P. M. van Putten", "Hilde E. Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036281.g001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lysozyme_MIC_levels_of_S_suis_/315809", "title"=>"Lysozyme MIC levels of <i>S. suis</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-30 01:36:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/645463"], "description"=>"<p>Strains 10-Δ<i>oatA</i>, 8067-Δ<i>oatA</i>, 8067-Δ<i>murMN</i>, 10::pGA14-<i>murMN</i> and wild type strain 10 and 8067 were spotted onto Colombia agar plates containing two-fold increasing concentrations of lysozyme. Growth was assessed 24 h later and MICs were determined. Green bars represent wild type and mutant derivatives of serotype 9 strain 8067 and blue bars represent wild type and mutant derivatives of serotype 2 strain 10. Values represent the mean of three independent observations. No error bars are displayed since the MIC values were identical in replicate experiments.</p>", "links"=>[], "tags"=>["mic", "levels", "oata", "murmn"], "article_id"=>315947, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Paul J. Wichgers Schreur", "Christian van Weeghel", "Johanna M. J. Rebel", "Mari A. Smits", "Jos P. M. van Putten", "Hilde E. Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036281.g002", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lysozyme_MIC_levels_of_OatA_and_MurMN_mutants_/315947", "title"=>"Lysozyme MIC levels of OatA and MurMN mutants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-30 01:39:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/645533"], "description"=>"<p>Lysozyme MIC of strain 10 passaged four times onto Colombia agar plates containing two-fold increasing concentrations of lysozyme (start concentration: 62.5 µg/ml). In general, within 4 passages the lysozyme MIC increased towards levels observed in natural lysozyme resistant strains (compare with <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036281#pone-0036281-g001\" target=\"_blank\">Figure 1</a>). * Lysozyme MIC level after sub-culturing lysozyme resistant strains in the absence of lysozyme. Values represent the MIC levels of an example of a selection procedure.</p>", "links"=>[], "tags"=>["mic", "levels", "10"], "article_id"=>316023, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Paul J. Wichgers Schreur", "Christian van Weeghel", "Johanna M. J. Rebel", "Mari A. Smits", "Jos P. M. van Putten", "Hilde E. Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036281.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lysozyme_MIC_levels_of_strain_10_after_passaging_/316023", "title"=>"Lysozyme MIC levels of strain 10 after passaging.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-30 01:40:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/645882"], "description"=>"<p><i>S. suis</i> bacteria are expected to resist the antimicrobial activity of lysozyme efficiently in the absence or reduced expression of capsule, in the presence of the peptidoglycan modifying enzyme OatA, and during reduced activity of autolysins. Loss of peptidoglycan stability, due to lysozyme digestion, makes <i>S. suis</i> increased vulnerable for osmotic pressure resulting in the flow of water into the bacterium's cytoplasm finally resulting in bacterial lysis.</p>", "links"=>[], "tags"=>["microbiology", "Biochemistry"], "article_id"=>316374, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Paul J. Wichgers Schreur", "Christian van Weeghel", "Johanna M. J. Rebel", "Mari A. Smits", "Jos P. M. van Putten", "Hilde E. Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036281.g007", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lysozyme_resistance_model_of_S_suis_/316374", "title"=>"Lysozyme resistance model of <i>S. suis</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-30 01:46:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/645768"], "description"=>"<p>Strain 10 (wild type), 10-LysR-1, 10-LysR-2, 10-Δ0475, 10-Δ<i>cps2EF</i> and 10-LysR-2-<i>cps2E</i> were grown exponentially in THB and visualised using crystal violet and light microscopy (A) and TEM (B).</p>", "links"=>[], "tags"=>["morphology", "lysozyme", "resistant"], "article_id"=>316260, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Paul J. Wichgers Schreur", "Christian van Weeghel", "Johanna M. J. Rebel", "Mari A. Smits", "Jos P. M. van Putten", "Hilde E. Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036281.g006", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bacterial_morphology_lysozyme_resistant_strains_/316260", "title"=>"Bacterial morphology lysozyme resistant strains.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-30 01:44:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/646003"], "description"=>"<p>Genomic differences observed between parent strain 10 and its selected lysozyme resistant derivatives 10-LysR1 and 10-LysR-2.</p>", "links"=>[], "tags"=>["differences", "observed", "10", "lysozyme", "resistant", "derivatives", "10-lysr1"], "article_id"=>316481, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Paul J. Wichgers Schreur", "Christian van Weeghel", "Johanna M. J. Rebel", "Mari A. Smits", "Jos P. M. van Putten", "Hilde E. Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036281.t002", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genomic_differences_observed_between_parent_strain_10_and_its_selected_lysozyme_resistant_derivatives_10_LysR1_and_10_LysR_2_/316481", "title"=>"Genomic differences observed between parent strain 10 and its selected lysozyme resistant derivatives 10-LysR1 and 10-LysR-2.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-04-30 01:48:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/332342", "https://ndownloader.figshare.com/files/332401"], "description"=>"<div><h3>Background</h3><p><em>Streptococcus suis</em> is an important infectious agent for pigs and occasionally for humans. The host innate immune system plays a key role in preventing and eliminating <em>S. suis</em> infections. One important constituent of the innate immune system is the protein lysozyme, which is present in a variety of body fluids and immune cells. Lysozyme acts as a peptidoglycan degrading enzyme causing bacterial lysis. Several pathogens have developed mechanisms to evade lysozyme-mediated killing. In the present study we compared the lysozyme sensitivity of various <em>S. suis</em> isolates and investigated the molecular basis of lysozyme resistance for this pathogen.</p> <h3>Results</h3><p>The lysozyme minimal inhibitory concentrations of a wide panel of <em>S. suis</em> isolates varied between 0.3 to 10 mg/ml. By inactivating the <em>oatA</em> gene in a serotype 2 and a serotype 9 strain, we showed that OatA-mediated peptidoglycan modification partly contributes to lysozyme resistance. Furthermore, inactivation of the <em>murMN</em> operon provided evidence that additional peptidoglycan crosslinking is not involved in lysozyme resistance in <em>S. suis</em>. Besides a targeted approach, we also used an unbiased approach for identifying factors involved in lysozyme resistance. Based on whole genome comparisons of a lysozyme sensitive strain and selected lysozyme resistant derivatives, we detected several single nucleotide polymorphisms (SNPs) that were correlated with the lysozyme resistance trait. Two SNPs caused defects in protein expression of an autolysin and a capsule sugar transferase. Analysis of specific isogenic mutants, confirmed the involvement of autolysin activity and capsule structures in lysozyme resistance of <em>S. suis</em>.</p> <h3>Conclusions</h3><p>This study shows that lysozyme resistance levels are highly variable among <em>S. suis</em> isolates and serotypes. Furthermore, the results show that lysozyme resistance in <em>S. suis</em> can involve different mechanisms including OatA-mediated peptidolycan modification, autolysin activity and capsule production.</p> </div>", "links"=>[], "tags"=>["lysozyme", "multifactorial"], "article_id"=>125631, "categories"=>["Biochemistry", "Microbiology"], "users"=>["Paul J. Wichgers Schreur", "Christian van Weeghel", "Johanna M. J. Rebel", "Mari A. Smits", "Jos P. M. van Putten", "Hilde E. Smith"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0036281.s001", "https://dx.doi.org/10.1371/journal.pone.0036281.s002"], "stats"=>{"downloads"=>3, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Lysozyme_Resistance_in_Streptococcus_suis_Is_Highly_Variable_and_Multifactorial/125631", "title"=>"Lysozyme Resistance in <em>Streptococcus suis</em> Is Highly Variable and Multifactorial", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-04-30 01:33:51"}

PMC Usage Stats | Further Information

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Relative Metric

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Net::HTTPTooManyRequests

Source
Scopus
Time
2019-08-27 19:05:45 UTC
Target URL
https://api.elsevier.com/content/search/index:SCOPUS?query=DOI(10.1371%2Fjournal.pone.0036281)
Trace

/app/models/concerns/networkable.rb:21:in `get_result'
/app/models/source.rb:165:in `get_data'
/app/models/retrieval_status.rb:47:in `perform_get_data'
/app/jobs/source_job.rb:52:in `block (2 levels) in perform'
/app/jobs/source_job.rb:51:in `block in perform'
/app/jobs/source_job.rb:35:in `each'
/app/jobs/source_job.rb:35:in `perform'