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Granadaene Photobleaching Reduces The Photochemistry and Photobiology, 20**, **: *–* Research Article Granadaene Photobleaching Reduces the Virulence and Increases Antimicrobial Susceptibility of Streptococcus agalactiae Sebastian Jusuf1, Pu-Ting Dong2 , Jie Hui3 , Erlinda R. Ulloa4, George Y. Liu5* and Ji-Xin Cheng1,2,3,6* 1Department of Biomedical Engineering, Boston University, Boston, MA 2Department of Chemistry, Boston University, Boston, MA 3Department of Electrical & Computer Engineering, Boston University, Boston, MA 4Department of Pediatrics, University of California Irvine School of Medicine, Irvine, CA 5Division of Pediatric Infectious Diseases, University of California San Diego School of Medicine, La Jolla, CA 6Photonics Center, Boston University, Boston, MA Received 8 November 2020, accepted 20 January 2021, DOI: 10.1111/php.13389 ABSTRACT infections has significantly decreased as a result of preventive intrapartum antibiotic prophylaxis (8,9), the rate of GBS infec- Streptococcus agalactiae, also known as Group B Streptococ- tion within nonpregnant adults has increased as evidenced by a cus (GBS), is increasingly recognized as a major cause of soft two-fold rise in incidence of invasive GBS disease in adults tissue and invasive diseases in the elderly and diabetic popu- between 1990 and 2007 (10). Compared to S. pneumoniae inva- lations. Antibiotics like penicillin are used with great fre- sive diseases (42 per 100 000), a leading cause of mortality in quency to treat these infections, although antimicrobial the elderly population, the incidence of GBS invasive disease resistance is increasing among GBS strains and underlines a among elderly is remarkable at 25 per 100 000, based on active, need for alternative methods not reliant on traditional antibi- population-based surveillance data from the ABCs Emerging otics. GBS granadaene pigment is related to the Infections Program Network on cases of and deaths associated hemolysin/cytolysin of GBS, which is critical for the patho- with infection due to several Gram-positive pathogens (7). genesis of GBS diseases. Here, we show that photobleaching As the rate of infection increases, treating GBS infection has granadaene dampens the hemolytic activity of GBS. Further- become more reliant on the usage of antibiotics like penicillin V, more, photobleaching of this antioxidant was found to ampicillin and daptomycin (11,12). However, even with optimal increase GBS susceptibility to killing by reactive oxygen spe- antibiotic treatment, management of skin infections can be diffi- cies like hydrogen peroxide. Treatment with light was also cult especially in patients suffering from diabetes (13). Com- shown to affect GBS membrane permeability and contribute pounding this therapeutic challenge, GBS has developed to increased susceptibility to the cell membrane-targeting resistance to commonly used antibiotics such as erythromycin antibiotic daptomycin. Overall, our study demonstrates dual and clindamycin and has also shown the capacity to develop effects of photobleaching on the virulence and antimicrobial resistance to b-lactam antibiotics, threatening future use of cur- susceptibility of GBS and suggests a novel approach for the rent first-line drugs (14,15). Because of these challenges, there is treatment of GBS infection. a growing need to develop novel GBS therapeutics that are less reliant on antibiotics. INTRODUCTION One of the key reasons why GBS is highly infectious is its multitude of virulence factors that endow it with the capability to Gram-positive streptococci are responsible for a wide variety of subvert suboptimal host defenses, allowing the bacterium to bet- medical conditions, ranging from more mild infections like strep ter adapt to its environment and cause severe infection (16). throat to more serious infections such as meningitis, myositis Some of these GBS virulence factors include the b-he- – and necrotizing fasciitis (2 4). Among the many species within molysin/cytolysin; the immune system evasion factor sialic acid the Streptococcus genus, Streptococcus agalactiae (commonly capsular polysaccharide; as well as antimicrobial resistance fac- b referred to as group B streptococcus or GBS) is a -hemolytic, tors such as penicillin-binding proteins and pili (17). Among all catalase negative facultative anaerobe which is best known for these different virulence factors, one of the most enigmatic is the causing neonatal invasive diseases (5,6). In recent years, there ornithine rhamno-polyene pigment known as granadaene, which has been a greater appreciation for GBS as a leading cause of is localized within the plasma membrane of GBS and found skin and soft tissue infections as well as invasive disease in the within 97% of human clinical GBS isolates (18,19). As the elderly and diabetic patients (7). While the risk of neonatal GBS source of the characteristic red color of GBS, granadaene con- tains a linear chain of twelve conjugated C=C bonds, providing *Corresponding authors email: [email protected] (George Liu) or [email protected] (Ji-Xin Cheng) the pigment with an absorption spectrum nearly identical to most This manuscript was previously submitted as a bioRxiv Pre-Print (1). carotenoids, with absorption peaks present at 430, 460, 490 and © 2021 American Society for Photobiology 1 2 Sebastian Jusuf et al. 520 nm (19). This similarity in conjugated double bonds pro- Broth was used for initial granadaene pigment extraction. For bacterial vides granadaene with antioxidant characteristics shared by tradi- susceptibility and hemolytic assays, a highly pigmented S. agalactiae D tional carotenoids and provides it with the ability to quench and strain (NCTC 10/84) and its nonpigmented isogenic CylE mutant were used (22). detoxify reactive oxygen species (ROS) such as hydrogen perox- Pigment extraction. Extraction of the granadaene pigment was ide (H2O2) and singlet oxygen and superoxide (20). Previous performed based on a modified extraction protocol published by Rosa- studies have shown that pigment increases GBS resistance to Fraile et al. (18). To summarize, GBS (ATCC 12386) was grown in 4 mL of New Granada Media/Strep B Carrot Broth (Z40, Hardy ROS like H2O2 and superoxide by 5- to 10-fold compared to pig- ° – fi fi Diagnostics) at 37 C for 48 72 h until the broth turned a rich orange-red ment-de cient mutants, as well as signi cantly contributing to color. Bacterial suspension was centrifuged and washed three times with the survival within phagocytes by shielding the bacteria from 1 mL of distilled water and two times with 1 mL of DMSO. Following oxidative damage (21). In addition to enhancing survival under washing, the bacterial pellet was resuspended in 0.5–1 mL of DMSO oxidative stress, studies have indicated a close relationship with 0.1% trifluoroacetic acid (TFA) overnight. The next day, the – between the pigment expression and hemolytic activity of GBS, suspension was centrifuged and the 0.5 1 mL of supernatant containing the extracted pigment was collected with measured OD490 ranging from both of which are controlled by the cyl operon (22,23). Recent 0.2 to 0.08, respectively. studies have indicated that the molecule responsible for pigmen- Photobleaching and spectroscopic measurements. Photobleaching and tation and the molecule responsible for hemolytic activity may subsequent absorbance measurements of extracted pigment and bacteria µ be one and the same, as findings have shown that increased pig- samples were performed by placing 90 L of extracted pigment suspended in DMSO/0.1% TFA (OD = 0.08) or concentrated GBS ment production correlates with increased hemolysin production 490 bacteria suspended in PBS (OD600 = 1.5) in a 96-well plate. Extracted À2 and that isolated and stabilized granadaene pigment exhibits pigment solution (OD490 = 0.08) was initially treated with 60 J cm of hemolytic activity, strongly indicating a close linkage between blue light ranging from 420 to 490 nm to determine the most effective the two virulence determinants (23–25). photobleaching wavelength based on the reduction of the 490 nm Based on the multiple conjugated bonds located within the absorbance peak. For 430 nm photobleaching, both extracted pigment solution (OD490 = 0.08) and concentrated GBS bacteria (OD600 = 1.5) structure of granadaene, the granadaene pigment is highly likely were exposed to 430 nm light for different time intervals to provide a to exhibit similar chemical reactivity to traditional carotenoids, range of light dosages (0, 30, 60, 120 J cmÀ2). The absorbance spectrum such as the increased photosensitivity and photodegradation of of each sample was then measured through a plate reader spectrometer. the carotenoid structure in response to near UV and blue light For Raman measurements, a Raman spectroscopy system (1221, LAB- RAM HR EVO, Horiba) with a 409 Olympus objective and an excita- exposure (26). Previous experiments have demonstrated that the tion wavelength of 532 nm was used to detect changes in pigment staphyloxanthin (STX) carotenoid pigment within methicillin-re- presence within GBS. Images were acquired under a 30 s acquisition sistant S. aureus (MRSA) is capable of undergoing photolysis time with a laser ND filter of 10%. Pigment-expressing GBS was concen- when exposed to 460 nm light. Such photolysis results in the trated in 50 µL of PBS, and a 2 µL droplet was aliquoted and sand- formation of pores within the cell membrane of MRSA that not wiched between two cover slides (48393-230, VWR International). Changes in pigment presence were determined by measuring the change only
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