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RNA thermosensors facilitate Streptococcus pneumoniae and Haemophilus influenzae immune evasion
Bacterial meningitis is a major cause of death and disability in children worldwide. Two human restricted respiratory pathogens, Streptococcus pneumoniae and Haemophilus influenzae, are the major causative agents of bacterial meningitis, attributing to 200,000 deaths annually. These pathogens are of...
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Published in: | PLoS pathogens 2021-04, Vol.17 (4), p.e1009513-e1009513 |
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description | Bacterial meningitis is a major cause of death and disability in children worldwide. Two human restricted respiratory pathogens, Streptococcus pneumoniae and Haemophilus influenzae, are the major causative agents of bacterial meningitis, attributing to 200,000 deaths annually. These pathogens are often part of the nasopharyngeal microflora of healthy carriers. However, what factors elicit them to disseminate and cause invasive diseases, remain unknown. Elevated temperature and fever are hallmarks of inflammation triggered by infections and can act as warning signals to pathogens. Here, we investigate whether these respiratory pathogens can sense environmental temperature to evade host complement-mediated killing. We show that productions of two vital virulence factors and vaccine components, the polysaccharide capsules and factor H binding proteins, are temperature dependent, thus influencing serum/opsonophagocytic killing of the bacteria. We identify and characterise four novel RNA thermosensors in S. pneumoniae and H. influenzae, responsible for capsular biosynthesis and production of factor H binding proteins. Our data suggest that these bacteria might have independently co-evolved thermosensing abilities with different RNA sequences but distinct secondary structures to evade the immune system. |
doi_str_mv | 10.1371/journal.ppat.1009513 |
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Two human restricted respiratory pathogens, Streptococcus pneumoniae and Haemophilus influenzae, are the major causative agents of bacterial meningitis, attributing to 200,000 deaths annually. These pathogens are often part of the nasopharyngeal microflora of healthy carriers. However, what factors elicit them to disseminate and cause invasive diseases, remain unknown. Elevated temperature and fever are hallmarks of inflammation triggered by infections and can act as warning signals to pathogens. Here, we investigate whether these respiratory pathogens can sense environmental temperature to evade host complement-mediated killing. We show that productions of two vital virulence factors and vaccine components, the polysaccharide capsules and factor H binding proteins, are temperature dependent, thus influencing serum/opsonophagocytic killing of the bacteria. We identify and characterise four novel RNA thermosensors in S. pneumoniae and H. influenzae, responsible for capsular biosynthesis and production of factor H binding proteins. Our data suggest that these bacteria might have independently co-evolved thermosensing abilities with different RNA sequences but distinct secondary structures to evade the immune system.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1009513</identifier><identifier>PMID: 33914847</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Bacteria ; Bacterial Capsules - metabolism ; Base Sequence - genetics ; Binding sites ; Biology and Life Sciences ; Biosensors ; Capsular polysaccharides ; Complement Factor H - metabolism ; Complement system ; Environment ; Gene expression ; Genetic aspects ; Haemophilus Infections - microbiology ; Haemophilus influenzae - genetics ; Haemophilus influenzae - immunology ; Haemophilus influenzae - physiology ; Health aspects ; Hemophilus influenzae ; Host-parasite relationships ; Immune evasion ; Immune response ; Macrophages ; Mathematical analysis ; Medicin och hälsovetenskap ; Medicine and Health Sciences ; Meningitis ; Meningitis, Bacterial - microbiology ; Nasopharynx - microbiology ; Operons ; Opsonophagocytosis ; Pathogens ; Phagocytosis ; Pneumococcal Infections - genetics ; Pneumococcal Infections - microbiology ; Polysaccharides ; Polysaccharides, Bacterial - metabolism ; Proteins ; Saccharides ; Statistics ; Streptococcus infections ; Streptococcus pneumoniae ; Streptococcus pneumoniae - immunology ; Streptococcus pneumoniae - physiology ; Survival ; Temperature ; Temperature effects ; Thermosensing ; Vaccines ; Virulence ; Virulence (Microbiology) ; Virulence factors ; Virulence Factors - metabolism</subject><ispartof>PLoS pathogens, 2021-04, Vol.17 (4), p.e1009513-e1009513</ispartof><rights>COPYRIGHT 2021 Public Library of Science</rights><rights>2021 Eichner et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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Two human restricted respiratory pathogens, Streptococcus pneumoniae and Haemophilus influenzae, are the major causative agents of bacterial meningitis, attributing to 200,000 deaths annually. These pathogens are often part of the nasopharyngeal microflora of healthy carriers. However, what factors elicit them to disseminate and cause invasive diseases, remain unknown. Elevated temperature and fever are hallmarks of inflammation triggered by infections and can act as warning signals to pathogens. Here, we investigate whether these respiratory pathogens can sense environmental temperature to evade host complement-mediated killing. We show that productions of two vital virulence factors and vaccine components, the polysaccharide capsules and factor H binding proteins, are temperature dependent, thus influencing serum/opsonophagocytic killing of the bacteria. 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Our data suggest that these bacteria might have independently co-evolved thermosensing abilities with different RNA sequences but distinct secondary structures to evade the immune system.</description><subject>Bacteria</subject><subject>Bacterial Capsules - metabolism</subject><subject>Base Sequence - genetics</subject><subject>Binding sites</subject><subject>Biology and Life Sciences</subject><subject>Biosensors</subject><subject>Capsular polysaccharides</subject><subject>Complement Factor H - metabolism</subject><subject>Complement system</subject><subject>Environment</subject><subject>Gene expression</subject><subject>Genetic aspects</subject><subject>Haemophilus Infections - microbiology</subject><subject>Haemophilus influenzae - genetics</subject><subject>Haemophilus influenzae - immunology</subject><subject>Haemophilus influenzae - physiology</subject><subject>Health aspects</subject><subject>Hemophilus influenzae</subject><subject>Host-parasite relationships</subject><subject>Immune evasion</subject><subject>Immune response</subject><subject>Macrophages</subject><subject>Mathematical analysis</subject><subject>Medicin och hälsovetenskap</subject><subject>Medicine and Health Sciences</subject><subject>Meningitis</subject><subject>Meningitis, Bacterial - 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genetics</topic><topic>Pneumococcal Infections - microbiology</topic><topic>Polysaccharides</topic><topic>Polysaccharides, Bacterial - metabolism</topic><topic>Proteins</topic><topic>Saccharides</topic><topic>Statistics</topic><topic>Streptococcus infections</topic><topic>Streptococcus pneumoniae</topic><topic>Streptococcus pneumoniae - immunology</topic><topic>Streptococcus pneumoniae - physiology</topic><topic>Survival</topic><topic>Temperature</topic><topic>Temperature effects</topic><topic>Thermosensing</topic><topic>Vaccines</topic><topic>Virulence</topic><topic>Virulence (Microbiology)</topic><topic>Virulence factors</topic><topic>Virulence Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Eichner, Hannes</creatorcontrib><creatorcontrib>Karlsson, Jens</creatorcontrib><creatorcontrib>Spelmink, Laura</creatorcontrib><creatorcontrib>Pathak, Anuj</creatorcontrib><creatorcontrib>Sham, Lok-To</creatorcontrib><creatorcontrib>Henriques-Normark, Birgitta</creatorcontrib><creatorcontrib>Loh, Edmund</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Science (Gale in Context)</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Virology and AIDS Abstracts</collection><collection>Health Medical collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection (Proquest) (PQ_SDU_P3)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>ProQuest Biological Science Journals</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>MEDLINE - 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Two human restricted respiratory pathogens, Streptococcus pneumoniae and Haemophilus influenzae, are the major causative agents of bacterial meningitis, attributing to 200,000 deaths annually. These pathogens are often part of the nasopharyngeal microflora of healthy carriers. However, what factors elicit them to disseminate and cause invasive diseases, remain unknown. Elevated temperature and fever are hallmarks of inflammation triggered by infections and can act as warning signals to pathogens. Here, we investigate whether these respiratory pathogens can sense environmental temperature to evade host complement-mediated killing. We show that productions of two vital virulence factors and vaccine components, the polysaccharide capsules and factor H binding proteins, are temperature dependent, thus influencing serum/opsonophagocytic killing of the bacteria. 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subjects | Bacteria Bacterial Capsules - metabolism Base Sequence - genetics Binding sites Biology and Life Sciences Biosensors Capsular polysaccharides Complement Factor H - metabolism Complement system Environment Gene expression Genetic aspects Haemophilus Infections - microbiology Haemophilus influenzae - genetics Haemophilus influenzae - immunology Haemophilus influenzae - physiology Health aspects Hemophilus influenzae Host-parasite relationships Immune evasion Immune response Macrophages Mathematical analysis Medicin och hälsovetenskap Medicine and Health Sciences Meningitis Meningitis, Bacterial - microbiology Nasopharynx - microbiology Operons Opsonophagocytosis Pathogens Phagocytosis Pneumococcal Infections - genetics Pneumococcal Infections - microbiology Polysaccharides Polysaccharides, Bacterial - metabolism Proteins Saccharides Statistics Streptococcus infections Streptococcus pneumoniae Streptococcus pneumoniae - immunology Streptococcus pneumoniae - physiology Survival Temperature Temperature effects Thermosensing Vaccines Virulence Virulence (Microbiology) Virulence factors Virulence Factors - metabolism |
title | RNA thermosensors facilitate Streptococcus pneumoniae and Haemophilus influenzae immune evasion |
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