Resident bacteria contribute to opportunistic infections of the respiratory tract

Abstract

Opportunistic pathogens frequently cause volatile infections in hosts with compromised immune systems or a disrupted normal microbiota. The commensalism of diverse microorganisms contributes to colonization resistance, which prevents the expansion of opportunistic pathogens. Following microbiota disruption, pathogens promptly adapt to altered niches and obtain growth advantages. Nevertheless, whether and how resident bacteria modulate the growth dynamics of invasive pathogens and the eventual outcome of such infections are still unclear. Here, we utilized birds as a model animal and observed a resident bacterium exacerbating the invasion of Avibacterium paragallinarum (previously Haemophilus paragallinarum) in the respiratory tract. We first found that negligibly abundant Staphylococcus chromogenes, rather than Staphylococcus aureus, played a dominant role in Av. paragallinarum-associated infectious coryza in poultry based on epidemic investigations and in vitro analyses. Furthermore, we determined that S. chromogenes not only directly provides the necessary nutrition factor nicotinamide adenine dinucleotide (NAD+) but also accelerates its biosynthesis and release from host cells to promote the survival and growth of Av. paragallinarum. Last, we successfully intervened in Av. paragallinarum-associated infections in animal models using antibiotics that specifically target S. chromogenes. Our findings show that opportunistic pathogens can hijack commensal bacteria to initiate infection and expansion and suggest a new paradigm to ameliorate opportunistic infections by modulating the dynamics of resident bacteria.

Development of an environmental contamination model to simulate the microbial bloom that occurs in commercial hatch cabinets

“…In mice, toxin production by S. aureus prevented elimination by the host immune system, which supported replication of Gram-negative bacteria in the lung and subsequent systemic infection ( Cohen et al, 2016 ). More recently, Wu et al (2021) demonstrated that S. chromogenes colonization in the upper respiratory tract of chickens promoted infection by Avibacterium paragallinarum, the etiologic agent of infectious coryza. These findings suggest that pioneer colonizers of the upper respiratory tract may facilitate infection and disease caused by opportunistic pathogens.…”

Streptococcus pyogenes can support or inhibit growth of Haemophilus influenzae by supplying or restricting extracellular NAD+

“…The plausibility of this hypothesis is supported by a study in chickens that reported infection of the upper airway by Avibacterium paragallinarum (previously Haemophilus paragallinarum ) was dependent on co-colonization with Staphylococcus chromogenes , which released NAD + , a required factor for A . paragallinarum growth [ 16 ]. In the present study, we found that a variety of bacteria, including species resident in the upper airway of humans, released NAD + that was readily detectable in extracellular culture fluid and which supported growth of H .…”

Commensal bacteria contribute to the growth of multidrug-resistant Avibacterium paragallinarum in chickens

“…In homeostasis, commensal bacteria exclude exogenous microorganisms and directly inhibit the growth of pathogens (Clark, 2020) resulting in the limited establishment of opportunistic pathogens such as A. paragallinarum in respiratory tract (Long et al, 2012). When host immunity is compromised, A. paragallinarum initiates colonization and invasion, which is facilitated by commensals like Gallibacterium anatis (Paudel et al, 2017), Ornithobacterium rhinotracheale (Morales-Erasto et al, 2016), and Staphylococcus chromogenes (Wu et al, 2021). Resident species constitute a new niche to allow A. paragallinarum colonization and virulence by providing public goods and disrupting host barriers (Hoare et al, 2021;Wu et al, 2021).…”

“…When host immunity is compromised, A. paragallinarum initiates colonization and invasion, which is facilitated by commensals like Gallibacterium anatis (Paudel et al, 2017), Ornithobacterium rhinotracheale (Morales-Erasto et al, 2016), and Staphylococcus chromogenes (Wu et al, 2021). Resident species constitute a new niche to allow A. paragallinarum colonization and virulence by providing public goods and disrupting host barriers (Hoare et al, 2021;Wu et al, 2021). Additionally, protection mediated by indigenous microbial communities including extensive horizontal gene transfer (McInnes et al, 2020) and antibiotic inactivation (Gjonbalaj et al, 2020) increases the antimicrobial tolerance and resistance of pathogens.…”