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4. Gene fitness landscape of group A streptococcus during necrotizing myositis

Author

Zhu, Luchang, Olsen, Randall J., Beres, Stephen B., Eraso, Jesus M., Saavedra, Matthew Ojeda, Kubiak, Samantha L., Cantu, Concepcion C., Jenkins, Leslie, Charbonneau, Amelia R.L., Waller, Andrew S., and Musser, James M.

Subjects
DNA sequencing -- Usage, Myositis -- Diagnosis -- Genetic aspects -- Patient outcomes, Necrotizing fasciitis, Primates, Genomics, Amino acids, Peptides, Skeletal muscle, Blood lipids, Transposons, Infection, Genomes, Genetic research, Health care industry
Abstract

Necrotizing fasciitis and myositis are devastating infections characterized by high mortality. Group A streptococcus (GAS) is a common cause of these infections, but the molecular pathogenesis is poorly understood. We report a genome-wide analysis using serotype M1 and M28 strains that identified GAS genes contributing to necrotizing myositis in nonhuman primates (NHP), a clinically relevant model. Using transposon-directed insertion-site sequencing (TraDIS), we identified 126 and 116 GAS genes required for infection by serotype M1 and M28 organisms, respectively. For both M1 and M28 strains, more than 25% of the GAS genes required for necrotizing myositis encode known or putative transporters. Thirteen GAS transporters contributed to both M1 and M28 strain fitness in NHP myositis, including putative importers for amino acids, carbohydrates, and vitamins and exporters for toxins, quorum-sensing peptides, and uncharacterized molecules. Targeted deletion of genes encoding 5 transporters confirmed that each isogenic mutant strain was significantly (P < 0.05) impaired in causing necrotizing myositis in NHPs. Quantitative reverse-transcriptase PCR (qRT-PCR) analysis showed that these 5 genes are expressed in infected NHP and human skeletal muscle. Certain substrate-binding lipoproteins of these transporters, such as Spy0271 and Spy1728, were previously documented to be surface exposed, suggesting that our findings have translational research implications., Introduction Necrotizing fasciitis, commonly known as the flesh-eating disease, is an invasive infection with very high rates of human morbidity and mortality (1). In severe cases, contiguous muscle may be [...]

Published
2019
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5. Integrated analysis of population genomics, transcriptomics and virulence provides novel insights into Streptococcus pyogenes pathogenesis

Author

Kachroo, Priyanka, Eraso, Jesus M., Beres, Stephen B., Olsen, Randall J., Zhu, Luchang, Nasser, Waleed, Bernard, Paul E., Cantu, Concepcion C., Saavedra, Matthew Ojeda, Arredondo, María José, Strope, Benjamin, Do, Hackwon, Kumaraswami, Muthiah, Vuopio, Jaana, Gröndahl-Yli-Hannuksela, Kirsi, Kristinsson, Karl G., Gottfredsson, Magnus, Pesonen, Maiju, Pensar, Johan, Davenport, Emily R., Clark, Andrew G., Corander, Jukka, Caugant, Dominique A., Gaini, Shahin, Magnussen, Marita Debess, Kubiak, Samantha L., Nguyen, Hoang A. T., Long, S. Wesley, Porter, Adeline R., DeLeo, Frank R., and Musser, James M.

Published
2019
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10. Genome Sequence and Comparative Microarray Analysis of Serotype M18 Group A Streptococcus Strains Associated with Acute Rheumatic Fever Outbreaks

Author

Smoot, James C., Barbian, Kent D., Van Gompel, Jamie J., Smoot, Laura M., Chaussee, Michael S., Sylva, Gail L., Sturdevant, Daniel E., Ricklefs, Stacy M., Porcella, Stephen F., Parkins, Larye D., Beres, Stephen B., Campbell, David S., Smith, Todd M., Zhang, Qing, Kapur, Vivek, Daly, Judy A., Veasy, L. George, and Musser, James M.

Published
2002

12. Evolutionary pathway to increased virulence and epidemic group A Streptococcus disease derived from 3,615 genome sequences

Author

Nasser, Waleed, Beres, Stephen B., Olsen, Randall J., Dean, Melissa A., Rice, Kelsey A., Long, S. Wesley, Kristinsson, Karl G., Gottfredsson, Magnus, Vuopio, Jaana, Raisanen, Kati, Caugant, Dominique A., Steinbakk, Martin, Low, Donald E., McGeer, Allison, Darenberg, Jessica, Henriques-Normark, Birgitta, Van Beneden, Chris A., Hoffmann, Steen, and Musser, James M.

Published
2014

13. A molecular trigger for intercontinental epidemics of group A Streptococcus

Author

Zhu, Luchang, Olsen, Randall J., Nasser, Waleed, Beres, Stephen B., Vuopio, Jaana, Kristinsson, Karl G., Gottfredsson, Magnus, Porter, Adeline R., DeLeo, Frank R., and Musser, James M.

Subjects
Epidemics, Streptococcus, Genetic polymorphisms -- Analysis -- Health aspects -- Research, Health care industry
Abstract

The identification of the molecular events responsible for strain emergence, enhanced virulence, and epidemicity has been a long-pursued goal in infectious diseases research. A recent analysis of 3,615 genomes of serotype M1 group A Streptococcus strains (the so-called 'flesh-eating' bacterium) identified a recombination event that coincides with the global M1 pandemic beginning in the early 1980s. Here, we have shown that the allelic variation that results from this recombination event, which replaces the chromosomal region encoding secreted NADase and streptolysin O, is the key driver of increased toxin production and enhanced infection severity of the M1 pandemic strains. Using isoallelic mutant strains, we found that 3 polymorphisms in this toxin gene region increase resistance to killing by human polymorphonuclear leukocytes, increase bacterial proliferation, and increase virulence in animal models of pharyngitis and necrotizing fasciitis. Genome sequencing of an additional 1,125 streptococcal strains and virulence studies revealed that a highly similar recombinational replacement event underlies an ongoing intercontinental epidemic of serotype M89 group A Streptococcus infections. By identifying the molecular changes that enhance upper respiratory tract fitness, increased resistance to innate immunity, and increased tissue destruction, we describe a mechanism that underpins epidemic streptococcal infections, which have affected many millions of people., Introduction One elusive goal in infectious diseases research is identification of the genetic changes and molecular mechanisms responsible for strain emergence, enhanced virulence, and epidemicity. This goal has practical importance [...]

Published
2015
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15. Polymorphisms in Regulator of Protease B (RopB) Alter Disease Phenotype and Strain Virulence of Serotype M3 Group A Streptococcus

Author

Olsen, Randall J., Laucirica, Daniel R., Watkins, M. Ebru, Feske, Marsha L., Garcia-Bustillos, Jesus R., Vu, Chau, Cantu, Concepcion, Shelburne, Samuel A., Fittipaldi, Nahuel, Kumaraswami, Muthiah, Shea, Patrick R., Flores, Anthony R., Beres, Stephen B., Lovgren, Maguerite, Tyrrell, Gregory J., Efstratiou, Androulla, Low, Donald E., Van Beneden, Chris A., and Musser, James M.

Published
2012
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18. Genetic evolution of invasive emm28 Streptococcus pyogenes strains and significant association with puerperal infections in young women in Finland

Author

Gröndahl-Yli-Hannuksela, Kirsi, Beres, Stephen B., Hyyryläinen, H.-L., Kallonen, Teemu, Musser, James M., and Vuopio, Jaana

Subjects
Adult, Aged, 80 and over, Whole-genome sequencing, Antigens, Bacterial, Adolescent, Streptococcus pyogenes, Group A streptococcus, Infant, Newborn, Infant, Bacteremia, Middle Aged, Article, Young Adult, Pregnancy, Child, Preschool, Streptococcal Infections, Humans, Puerperal Infection, Female, Puerperal sepsis, Child, Bacteraemic, Finland, Aged, Retrospective Studies
Abstract

Objectives Streptococcus pyogenes or group A streptococcus (GAS) is a human specific pathogen that annually infects over 700 million individuals. GAS strains of type emm28 are an abundant cause of invasive infections in Europe and North America. Methods We conducted a population-based study on bacteraemic emm28 GAS cases in Finland, from 1995 to 2015. Whole-genome sequencing (WGS) was used to genetically characterize the bacterial isolates. Bayesian analysis of the population structure was used to define genetic clades. Register-linkage analysis was performed to test for association of emm28 GAS with delivery- or postpartum-related infections. A genome-wide association study was used to search for DNA sequences associated with delivery or puerperal infections. Results Among 3060 bacteraemic cases reported during the study period, 714 were caused by emm28. Women comprised a majority of cases (59 %, 422/714), and were significantly over-represented (84.4 %, 162/192, p < 0.0001) among cases in the childbearing age group (20–40 years). Register-linkage analysis revealed strong association (p < 0.0001) of emm28 bacteraemias with delivery and puerperium. In this register-linkage analysis, 120 women with GAS bacteraemia were identified and linked to delivery, infections during delivery or puerperium time. Among these the proportion of cases caused by emm28 was significantly higher than any other emm type (55.8%, 67/120, p < 0.0001). Among the four genetic subclades identified, SC1B has dominated among the bacteraemic cases since 2000. Altogether 620 of 653 (94.9%) isolates belonged to SC1B. No specific sequence or genetic clade was found nonrandomly associated with delivery or puerperal infections. Conclusions Women of childbearing age were significantly overrepresented among bacteraemic emm28 GAS cases, and in particular were strongly associated with delivery and puerperium cases over the 21 years studied. The molecular mechanisms behind these associations are unclear and warrant further investigation.

Published
2020

19. Molecular Complexity of Successive Bacterial Epidemics Deconvoluted by Comparative Pathogenomics

Author

Beres, Stephen B., Carroll, Ronan K., Shea, Patrick R., Sitkiewicz, Izabela, Martinez-Gutierrez, Juan Carlos, Low, Donald E., McGeer, Allison, Willey, Barbara M., Green, Karen, Tyrrell, Gregory J., Goldman, Thomas D., Feldgarden, Michael, Birren, Bruce W., Fofanov, Yuriy, Boos, John, Wheaton, William D., Honisch, Christiane, Musser, James M., and Cantor, Charles R.

Published
2010
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20. Decreased Necrotizing Fasciitis Capacity Caused by a Single Nucleotide Mutation That Alters a Multiple Gene Virulence Axis

Author

Olsen, Randall J., Sitkiewicz, Izabela, Ayeras, Ara A., Gonulal, Vedia E., Cantu, Concepcion, Beres, Stephen B., Green, Nicole M., Lei, Benfang, Humbird, Tammy, Greaver, Jamieson, Chang, Ellen, Ragasa, Willie P., Montgomery, Charles A., Cartwright,, Joiner, McGeer, Allison, Low, Donald E., Whitney, Adeline R., Cagle, Philip T., Blasdel, Terry L., DeLeo, Frank R., Musser, James M., and Krause, Richard

Published
2010
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29. Group A Streptococcus emm gene types in pharyngeal isolates, Ontario, Canada, 2002-2010

Author

Shea, Patrick R., Ewbank, Amy L., Gonzalez-Lugo, Javier H., Martagon-Rosado, Alexandro J., Martinez-Gutierrez, Juan C., Rehman, Hina A., Serrano-Gonzalez, Monica, Fittipaldi, Nahuel, Beres, Stephen B., Flores, Anthony R., Low, Donald E., Willey, Barbara M., and Musser, James M.

Subjects
United States. Centers for Disease Control and Prevention, Infection -- Genetic aspects -- Health aspects, Bacterial genetics -- Health aspects, Health
Abstract

Group A Streptococcus (GAS) is a gram-positive bacterial pathogen responsible for ≅600 million cases of pharyngitis each year worldwide (1). The widespread prevalence of this disease results in considerable costs, [...]

Published
2011
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30. Naturally occurring single amino acid replacements in a regulatory protein alter streptococcal gene expression and virulence in mice

Author

Carroll, Ronan K., Shelburne, Samuel A., Olsen, Randall J., Suber, Bryce, Sahasrabhojane, Pranoti, Kumaraswami, Muthiah, Beres, Stephen B., Shea, Patrick R., Flores, Anthony R., and Musser, James M.

Subjects
Virulence (Microbiology) -- Research -- Genetic aspects, Gene expression -- Research -- Genetic aspects, Streptococcus -- Genetic aspects -- Research, Single nucleotide polymorphisms -- Research -- Genetic aspects, Health care industry
Abstract

Infection with different strains of the same species of bacteria often results in vastly different clinical out-comes. Despite extensive investigation, the genetic basis of microbial strain-specific virulence remains poorly understood. [...]

Published
2011
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32. Population Genomic Molecular Epidemiological Study of Macrolide-Resistant Streptococcus pyogenes in Iceland, 1995 to 2016: Identification of a Large Clonal Population with a pbp2x Mutation Conferring Reduced In Vitro β-Lactam Susceptibility

Author

Southon, Sara B., Beres, Stephen B., Kachroo, Priyanka, Saavedra, Matthew Ojeda, Erlendsdóttir, Helga, Haraldsson, Gunnsteinn, Yerramilli, Prasanti, Pruitt, Layne, Zhu, Luchang, Musser, James M., Kristinsson, Karl G., Læknadeild (HÍ), Faculty of Medicine (UI), Heilbrigðisvísindasvið (HÍ), School of Health Sciences (UI), Háskóli Íslands, and University of Iceland

Subjects
Antibiotic resistance, Streptococcus pyogenes, Molecular epidemiology, Sýkingar, Macrolides, Population genomics, Erfðarannsóknir, Sýklalyf
Abstract

Publisher's version (útgefin grein), Resistance to macrolide antibiotics is a global concern in the treatment of Streptococcus pyogenes (group A Streptococcus [GAS]) infections. In Iceland, since the detection of the first macrolide-resistant isolate in 1998, three epidemic waves of macrolide-resistant GAS infections have occurred, with peaks in 1999, 2004, and 2008. We conducted whole-genome sequencing of all 1,575 available GAS macrolide-resistant clinical isolates of all infection types collected at the national reference laboratory in Reykjavik, Iceland, from 1998 to 2016. Among 1,515 erythromycin-resistant isolates, 90.3% were of only three emm types, emm4 (n = 713), emm6 (n = 324), and emm12 (n = 332), with each being predominant in a distinct epidemic peak. The antibiotic efflux pump genes, mef(A) and msr(D), were present on chimeric mobile genetic elements in 99.3% of the macrolide-resistant isolates of these emm types. Of note, in addition to macrolide resistance, virtually all emm12 isolates had a single amino acid substitution in penicillin-binding protein PBP2X that conferred a 2-fold increased penicillin G and ampicillin MIC among the isolates tested. We conclude that each of the three large epidemic peaks of macrolide-resistant GAS infections occurring in Iceland since 1998 was caused by the emergence and clonal expansion of progenitor strains, with macrolide resistance being conferred predominantly by inducible Mef(A) and Msr(D) drug efflux pumps. The occurrence of emm12 strains with macrolide resistance and decreased beta-lactam susceptibility was unexpected and is of public health concern., This study was supported in part by the Fondren Foundation, Houston Methodist Hospital and Research Institute, and National Institutes of Health grants AI139369 and AI146771 (to J.M.M.).

Published
2020

33. Reduced in vitro susceptibility of Streptococcus pyogenes to beta-lactam antibiotics associated with mutations in the pbp2x gene is geographically widespread

Author

Musser, James M., Beres, Stephen B., Zhu, Luchang, Olsen, Randall J., Vuopio, Jaana, Hyyryläinen, Hanne-Leena, Gröndahl-Yli-Hannuksela, Kirsi, Kristinsson, Karl G., Darenberg, Jessica, Henriques-Normark, Birgitta, Hoffmann, Steen, Caugant, Dominque A., Smith, Andrew J., Lindsay, Diane S.J., Boragine, David, and Palzkill, Timothy

Abstract

Recently two related Streptococcus pyogenes strains with reduced susceptibility to ampicillin, amoxicillin and cefotaxime, antibiotics commonly used to treat S. pyogenes infections were reported. The two strains had the same nonsynonymous (amino acid-substituting) mutation in the pbp2x gene encoding penicillin-binding protein 2X (PBP2X). This concerning report led us to investigate our library of 7,025 genome sequences of type emm1, emm28, and emm89 S. pyogenes clinical strains recovered from intercontinental sources for mutations in pbp2x. We identified 137 strains that combined had 37 nonsynonymous mutations in 36 codons in pbp2x. Although to a lesser magnitude than the two previously published isolates, many of our strains had decreased susceptibility in vitro to multiple beta-lactam antibiotics. Many pbp2x mutations were found only in single strains, but 16 groups of two or more isolates of the same emm type had an identical amino acid replacement. Phylogenetic analysis showed that with one exception, strains of the same emm type with the same amino acid replacement were clonally related by descent. This finding indicates that strains with some amino acid changes in PBP2X can successfully spread to new human hosts and cause invasive infections. Mapping of the amino acid changes onto a three-dimensional structure of the related Streptococcus pneumoniae PBP2X suggests that some substitutions are located in regions functionally important in related pathogenic bacterial species. Decreased beta-lactam susceptibility is geographically widespread in strains of numerically common emm gene subtypes. Enhanced surveillance and further epidemiological and molecular genetic study of this potential emergent antimicrobial problem are warranted.

Published
2020

35. Population Genomic Molecular Epidemiological Study of Macrolide-Resistant Streptococcus pyogenes in Iceland, 1995 to 2016: Identification of a Large Clonal Population with a pbp2x Mutation Conferring Reduced In Vitro β-Lactam Susceptibility

Author

Southon, Sara B., primary, Beres, Stephen B., additional, Kachroo, Priyanka, additional, Saavedra, Matthew Ojeda, additional, Erlendsdóttir, Helga, additional, Haraldsson, Gunnsteinn, additional, Yerramilli, Prasanti, additional, Pruitt, Layne, additional, Zhu, Luchang, additional, Musser, James M., additional, and Kristinsson, Karl G., additional

Published
2020
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37. In vitro serial passage of Staphylococcus aureus: changes in psysiology, virulence factor production, and agr nucleotide sequence

Author

Somerville, Greg A., Beres, Stephen B., Fitzgerald, J. Ross, DeLeo, Frank R., Cole, Robert L., Hoff, Jessica S., and Musser, James M.

Subjects
Bacteriology -- Research, Nucleotides -- Physiological aspects, Staphylococcus aureus -- Genetic aspects, Toxic shock syndrome -- Causes of, Biological sciences
Abstract

Research has been conducted on Staphylococcus aureus strains, recovered from the patient with toxic shock syndrome, which have high aconitase activity. The hypothesis that the aconitase specific activity decreases over time during the in vitro passage has been examined and the effect of the serial passage on the growth and virulence factor production has been investigated.

Published
2002

38. Streptococcus pyogenes genes that promote pharyngitis in primates

Author

Zhu, Luchang, primary, Olsen, Randall J., additional, Beres, Stephen B., additional, Saavedra, Matthew Ojeda, additional, Kubiak, Samantha L., additional, Cantu, Concepcion C., additional, Jenkins, Leslie, additional, Waller, Andrew S., additional, Sun, Zhizeng, additional, Palzkill, Timothy, additional, Porter, Adeline R., additional, DeLeo, Frank R., additional, and Musser, James M., additional

Published
2020
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39. Population genomic molecular epidemiological study of macrolide resistant Streptococcus pyogenes in Iceland, 1995-2016: Identification of a large clonal population with a pbp2x mutation conferring reduced in vitro β-lactam susceptibility

Author

Southon, Sara B., primary, Beres, Stephen B., additional, Kachroo, Priyanka, additional, Saavedra, Matthew Ojeda, additional, Erlendsdóttir, Helga, additional, Haraldsson, Gunnsteinn, additional, Yerramilli, Prasanti, additional, Pruitt, Layne, additional, Zhu, Luchang, additional, Musser, James M., additional, and Kristinsson, Karl G., additional

Published
2020
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40. Genetic heterogeneity of the Spy1336/R28—Spy1337 virulence axis in Streptococcus pyogenes and effect on gene transcript levels and pathogenesis

Author

Eraso, Jesus M., primary, Kachroo, Priyanka, additional, Olsen, Randall J., additional, Beres, Stephen B., additional, Zhu, Luchang, additional, Badu, Traci, additional, Shannon, Sydney, additional, Cantu, Concepcion C., additional, Saavedra, Matthew Ojeda, additional, Kubiak, Samantha L., additional, Porter, Adeline R., additional, DeLeo, Frank R., additional, and Musser, James M., additional

Published
2020
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41. Reduced In Vitro Susceptibility of Streptococcus pyogenes to β-Lactam Antibiotics Associated with Mutations in the pbp2x Gene Is Geographically Widespread

Author

Musser, James M., primary, Beres, Stephen B., additional, Zhu, Luchang, additional, Olsen, Randall J., additional, Vuopio, Jaana, additional, Hyyryläinen, Hanne-Leena, additional, Gröndahl-Yli-Hannuksela, Kirsi, additional, Kristinsson, Karl G., additional, Darenberg, Jessica, additional, Henriques-Normark, Birgitta, additional, Hoffmann, Steen, additional, Caugant, Dominque A., additional, Smith, Andrew J., additional, Lindsay, Diane S. J., additional, Boragine, David M., additional, and Palzkill, Timothy, additional

Published
2020
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42. The serotype of type Ia and III group B streptococci is determined by the polymerasxe gene within the polycistronic capsule operon

Author

Chaffin, Donald O., Beres, Stephen B., Yim, Harry H., and Rubens, Craig E.

Subjects
Streptococcus agalactiae -- Genetic aspects, Microbial polysaccharides -- Physiological aspects, Immunospecificity -- Analysis, Genetic regulation -- Analysis, Biological sciences
Abstract

Results show that cpsIaH and cpsIIIH genes encode Ia and III capsular polysaccharide polymerases respectively, leading to the synthesis of type-specific capsular polysaccharides. Data point out that these polysaccharides aid in host immune defence mechanism in Streptococcus agalactiae.

Published
2000

43. Genetic heterogeneity of the Spy1336/R28 – Spy1337 Virulence Axis inStreptococcus pyogenesand Effect on Gene Transcript Levels and Pathogenesis

Author

Eraso, Jesus M., primary, Kachroo, Priyanka, additional, Olsen, Randall J., additional, Beres, Stephen B., additional, Zhu, Luchang, additional, Badu, Traci, additional, Shannon, Sydney, additional, Cantu, Concepcion C., additional, Saavedra, Matthew Ojeda, additional, Kubiak, Samantha L., additional, Porter, Adeline R., additional, DeLeo, Frank R., additional, and Musser, James M., additional

Published
2019
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45. Genomic analysis of emm59 group A Streptococcus invasive strains, United States

Author

Fittipaldi, Nahuel, Olsen, Randall J., Beres, Stephen B., Van Beneden, Chris, and Musser, James M.

Subjects
Epidemics -- Genetic aspects -- Health aspects -- Analysis, Medical research -- Health aspects -- Analysis, Medicine, Experimental -- Health aspects -- Analysis, Genes -- Health aspects -- Analysis, Infection -- Genetic aspects -- Health aspects -- Analysis, Health
Abstract

Group A Streptococcus (GAS) causes human diseases ranging in severity from uncomplicated pharyngitis to life-threatening necrotizing fasciitis (1). GAS strains have traditionally been classified based on a serologic reaction against [...]

Published
2012
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47. Gene fitness landscape of group A streptococcus during necrotizing myositis

Author

Zhu, Luchang, primary, Olsen, Randall J., additional, Beres, Stephen B., additional, Eraso, Jesus M., additional, Saavedra, Matthew Ojeda, additional, Kubiak, Samantha L., additional, Cantu, Concepcion C., additional, Jenkins, Leslie, additional, Charbonneau, Amelia R. L., additional, Waller, Andrew S., additional, and Musser, James M., additional

Published
2018
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