Increased Zinc Availability Enhances Initial Aggregation and Biofilm Formation of Streptococcus pneumoniae

Bacteria growing within biofilms are protected from antibiotics and the immune system. Within these structures, horizontal transfer of genes encoding virulence factors, and promoting antibiotic resistance occurs, making biofilms an extremely important aspect of pneumococcal colonization and persiste...

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Main Authors: Lindsey R. Brown, Rachel C. Caulkins, Tyler E. Schartel, Jason W. Rosch, Erin S. Honsa, Stacey Schultz-Cherry, Victoria A. Meliopoulos, Sean Cherry, Justin A. Thornton
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-06-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fcimb.2017.00233/full
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author Lindsey R. Brown
Rachel C. Caulkins
Tyler E. Schartel
Jason W. Rosch
Erin S. Honsa
Stacey Schultz-Cherry
Victoria A. Meliopoulos
Sean Cherry
Justin A. Thornton
author_facet Lindsey R. Brown
Rachel C. Caulkins
Tyler E. Schartel
Jason W. Rosch
Erin S. Honsa
Stacey Schultz-Cherry
Victoria A. Meliopoulos
Sean Cherry
Justin A. Thornton
author_sort Lindsey R. Brown
collection DOAJ
description Bacteria growing within biofilms are protected from antibiotics and the immune system. Within these structures, horizontal transfer of genes encoding virulence factors, and promoting antibiotic resistance occurs, making biofilms an extremely important aspect of pneumococcal colonization and persistence. Identifying environmental cues that contribute to the formation of biofilms is critical to understanding pneumococcal colonization and infection. Iron has been shown to be essential for the formation of pneumococcal biofilms; however, the role of other physiologically important metals such as copper, zinc, and manganese has been largely neglected. In this study, we investigated the effect of metals on pneumococcal aggregation and early biofilm formation. Our results show that biofilms increase as zinc concentrations increase. The effect was found to be zinc-specific, as altering copper and manganese concentrations did not affect biofilm formation. Scanning electron microscopy analysis revealed structural differences between biofilms grown in varying concentrations of zinc. Analysis of biofilm formation in a mutant strain lacking the peroxide-generating enzyme pyruvate oxidase, SpxB, revealed that zinc does not protect against pneumococcal H2O2. Further, analysis of a mutant strain lacking the major autolysin, LytA, indicated the role of zinc as a negative regulator of LytA-dependent autolysis, which could affect biofilm formation. Additionally, analysis of cell-cell aggregation via plating and microscopy revealed that high concentrations of zinc contribute to intercellular interaction of pneumococci. The findings from this study demonstrate that metal availability contributes to the ability of pneumococci to form aggregates and subsequently, biofilms.
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spelling doaj.art-8560e77c0d7843f89913826ac3dd46172022-12-21T23:50:25ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882017-06-01710.3389/fcimb.2017.00233264641Increased Zinc Availability Enhances Initial Aggregation and Biofilm Formation of Streptococcus pneumoniaeLindsey R. Brown0Rachel C. Caulkins1Tyler E. Schartel2Jason W. Rosch3Erin S. Honsa4Stacey Schultz-Cherry5Victoria A. Meliopoulos6Sean Cherry7Justin A. Thornton8Department of Biological Sciences, Mississippi State UniversityStarkville, MS, United StatesDepartment of Biological Sciences, Mississippi State UniversityStarkville, MS, United StatesDepartment of Biological Sciences, Mississippi State UniversityStarkville, MS, United StatesDepartment of Infectious Diseases, St. Jude Children's Research HospitalMemphis, TN, United StatesDepartment of Infectious Diseases, St. Jude Children's Research HospitalMemphis, TN, United StatesDepartment of Infectious Diseases, St. Jude Children's Research HospitalMemphis, TN, United StatesDepartment of Infectious Diseases, St. Jude Children's Research HospitalMemphis, TN, United StatesDepartment of Infectious Diseases, St. Jude Children's Research HospitalMemphis, TN, United StatesDepartment of Biological Sciences, Mississippi State UniversityStarkville, MS, United StatesBacteria growing within biofilms are protected from antibiotics and the immune system. Within these structures, horizontal transfer of genes encoding virulence factors, and promoting antibiotic resistance occurs, making biofilms an extremely important aspect of pneumococcal colonization and persistence. Identifying environmental cues that contribute to the formation of biofilms is critical to understanding pneumococcal colonization and infection. Iron has been shown to be essential for the formation of pneumococcal biofilms; however, the role of other physiologically important metals such as copper, zinc, and manganese has been largely neglected. In this study, we investigated the effect of metals on pneumococcal aggregation and early biofilm formation. Our results show that biofilms increase as zinc concentrations increase. The effect was found to be zinc-specific, as altering copper and manganese concentrations did not affect biofilm formation. Scanning electron microscopy analysis revealed structural differences between biofilms grown in varying concentrations of zinc. Analysis of biofilm formation in a mutant strain lacking the peroxide-generating enzyme pyruvate oxidase, SpxB, revealed that zinc does not protect against pneumococcal H2O2. Further, analysis of a mutant strain lacking the major autolysin, LytA, indicated the role of zinc as a negative regulator of LytA-dependent autolysis, which could affect biofilm formation. Additionally, analysis of cell-cell aggregation via plating and microscopy revealed that high concentrations of zinc contribute to intercellular interaction of pneumococci. The findings from this study demonstrate that metal availability contributes to the ability of pneumococci to form aggregates and subsequently, biofilms.http://journal.frontiersin.org/article/10.3389/fcimb.2017.00233/fullzincpneumococcuscell-cell interactionsbiofilmscolonization
spellingShingle Lindsey R. Brown
Rachel C. Caulkins
Tyler E. Schartel
Jason W. Rosch
Erin S. Honsa
Stacey Schultz-Cherry
Victoria A. Meliopoulos
Sean Cherry
Justin A. Thornton
Increased Zinc Availability Enhances Initial Aggregation and Biofilm Formation of Streptococcus pneumoniae
Frontiers in Cellular and Infection Microbiology
zinc
pneumococcus
cell-cell interactions
biofilms
colonization
title Increased Zinc Availability Enhances Initial Aggregation and Biofilm Formation of Streptococcus pneumoniae
title_full Increased Zinc Availability Enhances Initial Aggregation and Biofilm Formation of Streptococcus pneumoniae
title_fullStr Increased Zinc Availability Enhances Initial Aggregation and Biofilm Formation of Streptococcus pneumoniae
title_full_unstemmed Increased Zinc Availability Enhances Initial Aggregation and Biofilm Formation of Streptococcus pneumoniae
title_short Increased Zinc Availability Enhances Initial Aggregation and Biofilm Formation of Streptococcus pneumoniae
title_sort increased zinc availability enhances initial aggregation and biofilm formation of streptococcus pneumoniae
topic zinc
pneumococcus
cell-cell interactions
biofilms
colonization
url http://journal.frontiersin.org/article/10.3389/fcimb.2017.00233/full
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