The Variation of Nasal Microbiota Caused by Low Levels of Gaseous Ammonia Exposure in Growing Pigs

Abstract

Exposure to gaseous ammonia, even at low levels, can be harmful to pigs and human health. However, less is known about the effects of sustained exposure to gaseous ammonia on nasal microbiota colonization in growing pigs. A total of 120 Duroc×Landrace×Yorkshire pigs were housed in 24 separate chambers and continuously exposed to gaseous ammonia at 0,5, 10, 15, 20, and 25 ppm (four groups per exposure level) for 4 weeks. Then, we used high-throughput sequencing to perform 16S rRNA gene analysis in nasal swabs samples from 72 pigs ( n = 12). The results of the nasal microbiota analysis showed that an increase in ammonia concentration, especially at 20 and 25 ppm, decreased the alpha diversity and relative abundance of nasal microbiota. Proteobacteria, Firmicutes, Bacteroidetes, Actinobacteria , and Chloroflexi were the most abundant phyla. In addition, the relative abundances of 24 microbial genera significantly changed as the ammonia level increased. Four microbial genera ( Pseudomonas, Lactobacillus, Prevotella , and Bacteroides ) were significantly decreased at 25 ppm, while only two genera ( Moraxella and Streptococcus ) were increased at 25 ppm. PICRUSt analyses showed that the relative abundances of the nasal microbiota involved in cell motility, signal transduction, the nervous system, environmental adaptation, and energy and carbohydrate metabolism were significantly decreased, while genes involved in the immune system, endocrine system, circulatory system, immune system diseases and metabolism of vitamins, lipid, and amino acids were increased with increased ammonia levels. The results of in vivo tests showed that an increase in ammonia levels, especially an ammonia level of 25 ppm, caused respiratory tract injury and increase the number of Moraxella and Streptococcus species, while simultaneously decreasing respiratory immunity and growth performance, consistent with the increased presence of harmful bacteria identified by nasal microbiota analysis. Herein, this study also indicted that the threshold concentration of ammonia in pig farming is 20 ppm.

The porcine respiratory microbiome: recent insights and future challenges

“…In vivo testing showed that an increase in ammonia levels, especially above 25 ppm, significantly damaged tracheal mucosa and alveoli, and decreased growth performance [26]. In addition, ammonia levels above 25 ppm reduced the colonization of beneficial bacteria such as Lactobacillus and increased the number of Moraxella and Streptococcus species in the nasal cavities of exposed pigs [26]. Antimicrobial exposure is another key environmental factor that can affect the development of URT microbiome at early stages of life, especially because antimicrobials are widely used for control of post-weaning diarrhoea [28].…”

“…Ammonia emissions are known for their potential negative consequences on farming environments, the ecosystem, and human and animal health [ 26 ]. The concentration of gaseous ammonia in the farm environment has been shown to affect the porcine airway [ 27 ].…”

“…The concentration of gaseous ammonia in the farm environment has been shown to affect the porcine airway [ 27 ]. In vivo testing showed that an increase in ammonia levels, especially above 25 ppm, significantly damaged tracheal mucosa and alveoli, and decreased growth performance [ 26 ]. In addition, ammonia levels above 25 ppm reduced the colonization of beneficial bacteria such as Lactobacillus and increased the number of Moraxella and Streptococcus species in the nasal cavities of exposed pigs [ 26 ].…”

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

“…In healthy bovine individuals, the URT microbiota (based on nasal and nasopharyngeal swab samples) is dominated by Proteobacteria, a group of bacteria suggested to have high functional variability (Bradley and Pollard, 2017), followed by Tenericutes, Firmicutes and Bacteroidetes (Gaeta et al, 2017;McMullen et al, 2019). Proteobacteria, Firmicutes, and Bacteroidetes are the three most dominant phyla in the URT bacterial communities in piglets (Slifierz et al, 2015;Correa-Fiz et al, 2016;Wang et al, 2019).…”

“…In cows and feedlot cattle, several studies have reported how a healthy respiratory microbiota is established in the airways and surveyed which host and environmental factors drive it (Timsit et al, 2016;Hall et al, 2017;Holman et al, 2017;Nicola et al, 2017;Zeineldin et al, 2017a;Holman et al, 2018;Stroebel et al, 2018;Amat et al, 2019;McMullen et al, 2020;Zeineldin et al, 2020a). Analogously, predicting when and how respiratory microbiome breaks down is at the heart of several studies in swine (Cortes et al, 2018;Zeineldin et al, 2018;Jakobsen et al, 2019;Megahed et al, 2019;Mou et al, 2019;Wang et al, 2019;Pirolo et al, 2021). For instance, it appears as though that during weaning, several microorganisms act synergistically to mediate the BRDC (Gaeta et al, 2017;Klima et al, 2019;McMullen et al, 2019;Zeineldin et al, 2019) and PRDC (Wang et al, 2018;Li et al, 2021).…”