Bacterial Stabilization of a Panel of Picornaviruses

Aguilera, Elizabeth R.; Nguyen, Y; Sasaki, Jun; Pfeiffer, Julie K.

doi:10.1128/msphere.00183-19

Cited by 43 publications

(64 citation statements)

References 33 publications

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“…Interactions with bacteria have previously been demonstrated to promote the stability of picornaviruses (15,16) and reoviruses (16,17). We hypothesized that bacterial stabilization of environmental IAV via direct interactions may be one mechanism that the virus exploits to retain infectivity following release into the environment.…”

Section: Resultsmentioning

confidence: 99%

Respiratory Bacteria Stabilize and Promote Airborne Transmission of Influenza A Virus

et al. 2020

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Influenza A virus (IAV) is a major pathogen of the human respiratory tract, where the virus coexists and interacts with bacterial populations comprising the respiratory tract microbiome. Synergies between IAV and respiratory bacterial pathogens promote enhanced inflammation and disease burden that exacerbate morbidity and mortality. We demonstrate that direct interactions between IAV and encapsulated bacteria commonly found in the respiratory tract promote environmental stability and infectivity of IAV. Antibiotic-mediated depletion of the respiratory bacterial flora abrogated IAV transmission in ferret models, indicating that these virus-bacterium interactions are operative for airborne transmission of IAV. Restoring IAV airborne transmission in antibiotic-treated ferrets by coinfection with Streptococcus pneumoniae confirmed a role for specific members of the bacterial respiratory community in promoting IAV transmission. These results implicate a role for the bacterial respiratory flora in promoting airborne transmission of IAV. IMPORTANCE Infection with influenza A virus (IAV), especially when complicated with a secondary bacterial infection, is a leading cause of global mortality and morbidity. Gaining a greater understanding of the transmission dynamics of IAV is important during seasonal IAV epidemics and in the event of a pandemic. Direct bacterium-virus interactions are a recently appreciated aspect of infectious disease biology. Direct interactions between IAV and specific bacterial species of the human upper respiratory tract were found to promote the stability and infectivity of IAV during desiccation stress. Viral environmental stability is an important aspect during transmission, suggesting a potential role for bacterial respiratory communities in IAV transmission. Airborne transmission of IAV was abrogated upon depletion of nasal bacterial flora with topical antibiotics. This defect could be functionally complemented by S. pneumoniae coinfection. These data suggest that bacterial coinfection may be an underappreciated aspect of IAV transmission dynamics.

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Section: Resultsmentioning

confidence: 99%

Respiratory Bacteria Stabilize and Promote Airborne Transmission of Influenza A Virus

et al. 2020

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“…Direct binding to gram-positive and gram-negative bacteria enhances the thermostability of poliovirus [10], Coxsackievirus B3 [5], HNoV [7,8], and reovirus [9], whereas the thermostability of Mengo and Aichi picornaviruses is strengthened by gram-positive and gram-negative bacteria, respectively [5]. Interestingly, both gram-positive and gram-negative bacteria also provide protection from bleach treatment to Aichi, Mengo, and poliovirus [5]. Moreover, binding of HNoV to HBGAs protects the virus from heat stress [8].…”

Section: Bacteria and Bacterial Components Influence Virion Stabilitymentioning

confidence: 99%

Virus interactions with bacteria: Partners in the infectious dance

Neu

Mainou

2020

PLoS Pathog

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The outcome of viral infection depends on the interplay between host factors and the environment. Host factors, like the expression of viral receptors, convey permissiveness to infection, define tropism, regulate antiviral immune responses, determine viral clearance, and spread. The host microbiota, the constellation of microbes inhabiting an organism, also plays a key role in the outcome of infection. Microbes and microbial products can directly interact with viral particles. Our understanding of how the microbiota impacts virus infection is largely limited to the bacterial component of the microbiota. Although bacteria do not support eukaryotic virus infection, they can promote viral fitness by enhancing virion stability, promoting infection of eukaryotic cells, and increasing coinfection rates. Virus binding of bacteria can also impact bacterial biology, including bacterial adherence to eukaryotic cells. These interactions can also indirectly affect the host response to viral infection. In this Pearl, we focus on how direct and indirect interactions between viruses and bacteria impact viral biology and touch on recent findings that illustrate how bacterial biology can also be impacted by interactions with eukaryotic viruses (Fig 1).

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“…Human rotavirus and norovirus interact with polymorphic human histo-blood group antigens (HBGAs), and this interaction is thought to be important for infection (32). LPS stabilizes coxsackievirus B3 (CVB3) in vitro, but CVB3 is more sensitive to microbiota perturbation than poliovirus (11,12), indicating that it may have distinct glycan binding specificity. Bacterial LPS and peptidoglycan also increase reovirus thermostability (33), but the detailed glycan binding specificity is unclear.…”

Section: Discussionmentioning

confidence: 99%

“…We found that long N-acetylglucosamine (GlcNAc)containing polysaccharides can stabilize poliovirus but that a six-unit GlcNAc oligosaccharide, GlcNAc6, could not. Recent comparison studies of poliovirus with other members of the Picornaviridae, such as coxsackievirus B3, Aichi virus, and mengovirus, revealed shared and distinct effects of bacteria on virion stability (12).…”

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confidence: 99%

Use of a Glycan Library Reveals a New Model for Enteric Virus Oligosaccharide Binding and Virion Stabilization

Lehrman

Pfeiffer

2020

J Virol

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Enteric viruses infect the gastrointestinal tract, and bacteria can promote replication and transmission of several enteric viruses. Viruses can be inactivated by exposure to heat or bleach, but poliovirus, coxsackievirus B3, and reovirus can be stabilized by bacteria or bacterial polysaccharides, limiting inactivation and aiding transmission. We previously demonstrated that certain N-acetylglucosamine (GlcNAc)-containing polysaccharides can stabilize poliovirus. However, the detailed virus-glycan binding specificity and glycan chain length requirements, and thus the mechanism of virion stabilization, have been unclear. A previous limitation was our lack of defined-length glycans to probe mechanisms and consequences of virus-glycan interactions. Here, we generated a panel of polysaccharides and oligosaccharides to determine the properties required for binding and stabilization of poliovirus. Poliovirus virions are nonenveloped icosahedral 30-nm particles with 60 copies of each of four capsid proteins, VP1 to VP4. VP1 surrounds the 5-fold axis, and our past work indicates that this region likely contains the glycan binding site. We found that relatively short GlcNAc oligosaccharides, such as a six-unit GlcNAc oligomer, can bind poliovirus but fail to enhance virion stability. Virion stabilization required binding of long GlcNAc polymers of greater than 20 units. Our data suggest a model where GlcNAc polymers of greater than 20 units bind and bridge adjacent 5-fold axes, thus aiding capsid rigidity and stability. This study provides a deeper understanding of enteric virus-bacterial glycan interactions, which are important for virion environmental stability and transmission. IMPORTANCE Enteric viruses are transmitted through the fecal-oral route, but how enteric viruses survive in the environment is unclear. Previously, we found that bacterial polysaccharides enhance poliovirus stability against heat or bleach inactivation, but the specific molecular requirements have been unknown. Here, we showed that certain short-chain oligosaccharides can bind to poliovirus but do not increase virion stability. Long-chain polysaccharides bind and may bridge adjacent sites on the viral surface, thus increasing capsid rigidity and stability. This work defines the unique interactions of poliovirus and glycans, which provides insight into virion environmental stability and transmission.

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Bacterial Stabilization of a Panel of Picornaviruses

Cited by 43 publications

References 33 publications

Respiratory Bacteria Stabilize and Promote Airborne Transmission of Influenza A Virus

Respiratory Bacteria Stabilize and Promote Airborne Transmission of Influenza A Virus

Virus interactions with bacteria: Partners in the infectious dance

Use of a Glycan Library Reveals a New Model for Enteric Virus Oligosaccharide Binding and Virion Stabilization

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