The Microbiota Contributes to the Control of Highly Pathogenic H5N9 Influenza Virus Replication in Ducks

Abstract

Ducks usually show little or no clinical signs following highly pathogenic avian influenza virus infection. In order to analyze whether the microbiota could contribute to the control of influenza virus replication in ducks, we used a broad-spectrum oral antibiotic treatment to deplete the microbiota before infection with a highly pathogenic H5N9 avian influenza virus. Antibiotic-treated ducks and nontreated control ducks did not show any clinical signs following H5N9 virus infection. We did not detect any significant difference in virus titers neither in the respiratory tract nor in the brain nor spleen. However, we found that antibiotic-treated H5N9 virus-infected ducks had significantly increased intestinal virus excretion at days 3 and 5 postinfection. This was associated with a significantly decreased antiviral immune response in the intestine of antibiotic-treated ducks. Our findings highlight the importance of an intact microbiota for an efficient control of avian influenza virus replication in ducks. IMPORTANCE Ducks are frequently infected with avian influenza viruses belonging to multiple subtypes. They represent an important reservoir species of avian influenza viruses, which can occasionally be transmitted to other bird species or mammals, including humans. Ducks thus have a central role in the epidemiology of influenza virus infection. Importantly, ducks usually show little or no clinical signs even following infection with a highly pathogenic avian influenza virus. We provide evidence that the microbiota contributes to the control of influenza virus replication in ducks by modulating the antiviral immune response. Ducks are able to control influenza virus replication more efficiently when they have an intact intestinal microbiota. Therefore, maintaining a healthy microbiota by limiting perturbations to its composition should contribute to the prevention of avian influenza virus spread from the duck reservoir.

Modulation of gut microbiota protects against viral respiratory tract infections: a systematic review of animal and clinical studies

“…A total of thirteen studies investigated the influence of commensal gut microbiota on the outcomes of viral RTIs in animal models (Table 4 ). Of these studies, ten focused on influenza virus [ 8 , 65 , 66 , 68 , 73 , 75 – 79 ], and the remaining studies were on RSV [ 80 ], parainfluenza virus [ 64 ] and avian influenza virus [ 81 ].…”

Host factors drive the within-host competition between highly and low pathogenic H5N8 avian influenza viruses

“…We suggest that the more pronounced antiviral innate immune response observed in ducks compared to chickens may impact the H5N8 HP minority variant more severely in ducks than in chickens. Admittedly, the differential outcome of H5N8 HP and H5N8 LP co-infections in chickens and ducks may also depend on other host factors, including microbiota composition or receptor distribution (Figueroa et al, 2020; Hiono et al, 2016).…”

The Airway Pathobiome in Complex Respiratory Diseases: A Perspective in Domestic Animals

“…In another study developed in chickens, Lactobacillus salivarius intake alleviated lung inflammation injury caused by Mycoplasma gallisepticum infection and increased host defense against Escherichia coli by improved gut microbiota composition (Wang et al, 2021). Antibiotic-treated ducks had increased levels of intestinal highly pathogenic avian influenza virus (HPAIV) of H5N9 subtype associated with a reduced antiviral immune response, but no higher viral titers in the respiratory tract (Figueroa et al, 2020). Finally, the oral administration of E. coli O86:B7 expressing high levels of galactose-a-1,3-galactose (a-Gal) in turkeys was found to abrogate anti-a-Gal IgA response in lungs and to protect against experimental Aspergillus fumigatus infection (Mateos Hernańdez et al, 2020).…”