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.
Highlights
Microbial communities coevolved with hosts are abundant on the surface of their bodies and the respiratory and gastrointestinal tracts
Secondary bacterial infections are common in clinical practice, whereas the growth dynamics of each individual in such coinfections are still complicated and elusive
Our results indicate that resident bacteria in the respiratory tract can promote the invasion and replication of opportunistic pathogens, and modulation of commensal bacterial dynamics may be an alternative strategy to prevent and control such infections
Summary
Microbial communities coevolved with hosts are abundant on the surface of their bodies and the respiratory and gastrointestinal tracts. The communities consist of trillions of commensal microorganisms, termed the microbiota, periodically interacting with various pathogenic invaders. Bacteroides species, comprising a predominant genus in the intestinal tract, promote the replication and expression of virulence genes of Escherichia coli [3, 4]. Staphylococcus aureus can prevent clearance by macrophages through the secretion of α-toxin, resulting in the expansion of opportunistic pathogens [5]. Collateral damage to the intestinal microbiota by oral antibiotics and invasive viruses renders hosts susceptible to Clostridium difficile [6] and Haemophilus spp. Similar to the well-characterized modulation of bacterial dynamics in the gut, we suspected that opportunistic bacteria might utilize resident bacteria to initiate colonization and invasion in the respiratory tract
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