Molecular Basis for the Evolution of Species-Specific Hemoglobin Capture by <named-content content-type="genus-species">Staphylococcus aureus</named-content>

ABSTRACT Metals are a limiting resource for pathogenic bacteria and must be scavenged from host proteins. Hemoglobin provides the most abundant source of iron in the human body and is required by several pathogens to cause invasive disease. However, the consequences of hemoglobin evolution for bacte...

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Autores principales:	Jacob E. Choby, Hanna B. Buechi, Allison J. Farrand, Eric P. Skaar, Matthew F. Barber
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Staphylococcus aureus evolution heme transport hemoglobin host-pathogen interactions iron acquisition Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/1ffa2eb9911b43c3946feb116ac169b2
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spelling	oai:doaj.org-article:1ffa2eb9911b43c3946feb116ac169b22021-11-15T15:52:19ZMolecular Basis for the Evolution of Species-Specific Hemoglobin Capture by <named-content content-type="genus-species">Staphylococcus aureus</named-content>10.1128/mBio.01524-182150-7511https://doaj.org/article/1ffa2eb9911b43c3946feb116ac169b22018-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01524-18https://doaj.org/toc/2150-7511ABSTRACT Metals are a limiting resource for pathogenic bacteria and must be scavenged from host proteins. Hemoglobin provides the most abundant source of iron in the human body and is required by several pathogens to cause invasive disease. However, the consequences of hemoglobin evolution for bacterial nutrient acquisition remain unclear. Here we show that the α- and β-globin genes exhibit strikingly parallel signatures of adaptive evolution across simian primates. Rapidly evolving sites in hemoglobin correspond to binding interfaces of IsdB, a bacterial hemoglobin receptor harbored by pathogenic Staphylococcus aureus. Using an evolution-guided experimental approach, we demonstrate that the divergence between primates and staphylococcal isolates governs hemoglobin recognition and bacterial growth. The reintroduction of putative adaptive mutations in α- or β-globin proteins was sufficient to impair S. aureus binding, providing a mechanism for the evolution of disease resistance. These findings suggest that bacterial hemoprotein capture has driven repeated evolutionary conflicts with hemoglobin during primate descent. IMPORTANCE During infection, bacteria must steal metals, including iron, from the host tissue. Therefore, pathogenic bacteria have evolved metal acquisition systems to overcome the elaborate processes mammals use to withhold metal from pathogens. Staphylococcus aureus uses IsdB, a hemoglobin receptor, to thieve iron-containing heme from hemoglobin within human blood. We find evidence that primate hemoglobin has undergone rapid evolution at protein surfaces contacted by IsdB. Additionally, variation in the hemoglobin sequences among primates, or variation in IsdB of related staphylococci, reduces bacterial hemoglobin capture. Together, these data suggest that S. aureus has evolved to recognize human hemoglobin in the face of rapid evolution at the IsdB binding interface, consistent with repeated evolutionary conflicts in the battle for iron during host-pathogen interactions.Jacob E. ChobyHanna B. BuechiAllison J. FarrandEric P. SkaarMatthew F. BarberAmerican Society for MicrobiologyarticleStaphylococcus aureusevolutionheme transporthemoglobinhost-pathogen interactionsiron acquisitionMicrobiologyQR1-502ENmBio, Vol 9, Iss 6 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Staphylococcus aureus evolution heme transport hemoglobin host-pathogen interactions iron acquisition Microbiology QR1-502
spellingShingle	Staphylococcus aureus evolution heme transport hemoglobin host-pathogen interactions iron acquisition Microbiology QR1-502 Jacob E. Choby Hanna B. Buechi Allison J. Farrand Eric P. Skaar Matthew F. Barber Molecular Basis for the Evolution of Species-Specific Hemoglobin Capture by <named-content content-type="genus-species">Staphylococcus aureus</named-content>
description	ABSTRACT Metals are a limiting resource for pathogenic bacteria and must be scavenged from host proteins. Hemoglobin provides the most abundant source of iron in the human body and is required by several pathogens to cause invasive disease. However, the consequences of hemoglobin evolution for bacterial nutrient acquisition remain unclear. Here we show that the α- and β-globin genes exhibit strikingly parallel signatures of adaptive evolution across simian primates. Rapidly evolving sites in hemoglobin correspond to binding interfaces of IsdB, a bacterial hemoglobin receptor harbored by pathogenic Staphylococcus aureus. Using an evolution-guided experimental approach, we demonstrate that the divergence between primates and staphylococcal isolates governs hemoglobin recognition and bacterial growth. The reintroduction of putative adaptive mutations in α- or β-globin proteins was sufficient to impair S. aureus binding, providing a mechanism for the evolution of disease resistance. These findings suggest that bacterial hemoprotein capture has driven repeated evolutionary conflicts with hemoglobin during primate descent. IMPORTANCE During infection, bacteria must steal metals, including iron, from the host tissue. Therefore, pathogenic bacteria have evolved metal acquisition systems to overcome the elaborate processes mammals use to withhold metal from pathogens. Staphylococcus aureus uses IsdB, a hemoglobin receptor, to thieve iron-containing heme from hemoglobin within human blood. We find evidence that primate hemoglobin has undergone rapid evolution at protein surfaces contacted by IsdB. Additionally, variation in the hemoglobin sequences among primates, or variation in IsdB of related staphylococci, reduces bacterial hemoglobin capture. Together, these data suggest that S. aureus has evolved to recognize human hemoglobin in the face of rapid evolution at the IsdB binding interface, consistent with repeated evolutionary conflicts in the battle for iron during host-pathogen interactions.
format	article
author	Jacob E. Choby Hanna B. Buechi Allison J. Farrand Eric P. Skaar Matthew F. Barber
author_facet	Jacob E. Choby Hanna B. Buechi Allison J. Farrand Eric P. Skaar Matthew F. Barber
author_sort	Jacob E. Choby
title	Molecular Basis for the Evolution of Species-Specific Hemoglobin Capture by <named-content content-type="genus-species">Staphylococcus aureus</named-content>
title_short	Molecular Basis for the Evolution of Species-Specific Hemoglobin Capture by <named-content content-type="genus-species">Staphylococcus aureus</named-content>
title_full	Molecular Basis for the Evolution of Species-Specific Hemoglobin Capture by <named-content content-type="genus-species">Staphylococcus aureus</named-content>
title_fullStr	Molecular Basis for the Evolution of Species-Specific Hemoglobin Capture by <named-content content-type="genus-species">Staphylococcus aureus</named-content>
title_full_unstemmed	Molecular Basis for the Evolution of Species-Specific Hemoglobin Capture by <named-content content-type="genus-species">Staphylococcus aureus</named-content>
title_sort	molecular basis for the evolution of species-specific hemoglobin capture by <named-content content-type="genus-species">staphylococcus aureus</named-content>
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/1ffa2eb9911b43c3946feb116ac169b2
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Molecular Basis for the Evolution of Species-Specific Hemoglobin Capture by <named-content content-type="genus-species">Staphylococcus aureus</named-content>

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