The Indoor-Air Microbiota of Pig Farms Drives the Composition of the Pig Farmers' Nasal Microbiota in a Season-Dependent and Farm-Specific Manner

Abstract

Prior studies have demonstrated an influence of the built environment on the human nasal microbiota. However, very little is known about the influences of working on a pig farm on the human nasal microbiota. We longitudinally collected samples from 30 pig farms (air and nasal swabs from humans and pigs) in Switzerland from 2014 to 2015. As controls, nasal swabs from cow farmers and individuals with no contact with farm animals were included. An analysis of the microbiota for all samples (n = 609) was performed based on 16S rRNA gene sequencing (MiSeq) and included the investigations of source-sink dynamics. The numbers of indoor airborne particles and bacterial loads in pig farms were also investigated and were highest in winter. Similarly, the microbiota analyses revealed that the alpha diversity values of the nares of pig farmers were increased in winter in contrast to those of samples from the nonexposed controls, which displayed low alpha diversity values throughout the seasons. Source-sink analyses revealed that bacteria from the noses of pigs are more commonly coidentified within the pig farmers' microbiota in winter but to a less extent in summer. In addition, in winter, there was a stronger intrasimilarity for samples that originated from the same farm than for samples from different farms, and this farm specificity was partially or completely lost in spring, summer, and fall. In conclusion, in contrast to nonexposed controls, a pig farmer's nasal microbiota is dynamic, as the indoor-air microbiota of pig farms drives the composition of the pig farmer's nasal microbiota in a season-dependent manner.IMPORTANCE The airborne microbiota of pig farms poses a potential health hazard and impacts both livestock and humans working in this environment. Therefore, a more thorough understanding of the microbiota composition and dynamics in this setting is needed. This study was of a prospective design (12 months) and used samples from different sites. This means that the microbiota of air, animals (pigs), and humans was simultaneously investigated. Our findings highlight that the potential health hazard might be particularly high in winter compared to that in summer.

Keywords: airborne microbiota; nasal microbiota; occupational exposure; pig farmers; seasonal variation.

FIG 1

Particle and bacterial loads inside pig confinement buildings throughout the year. The mass of particles in the inhalable fraction (log transformed) (A) and 16S rRNA gene copy numbers (log transformed) (B) are indicated. *, P < 0.05; **, P < 0.01; ***, P < 0.001.

FIG 2

Flow chart of sample processing, including information on excluded samples. *, two cow farmers and nine nonexposed individuals were fully excluded from the study, as there was only one high-quality sample per individual left after sample processing.

FIG 3

Longitudinal taxonomy plots. Cumulative bar charts comparing relative abundances of samples from pigs, air, pig farmers, cow farmers, and nonexposed individuals throughout the seasons at the phylum level (A) and family level (B) are illustrated. Clostridiales here represents all families of this order except Clostridiaceae.

FIG 4

Alpha diversity analyses of samples from pigs, air, pig farmers, cow farmers, and nonexposed individuals throughout the seasons. This is illustrated by the differences of richness (observed sequence variants [SVs]) (A) and Shannon diversity indices (B) based on season for each sample type. The lines represent the means and the shaded areas the 95% confidence intervals. *, P < 0.05; **, P < 0.01; ***, P < 0.001.

FIG 5

Contribution of pigs’ nasal microbiomes as potential sources of a pig farmer’s microbial assemblage in each season using Bayesian source tracker analysis. (A) The proportions of each pig farmer’s microbiome coming from pigs, nonexposed individuals, and unknown sources are indicated. (B) A separate analysis revealing the proportions of each pig farmer’s microbiome coming from the air and unknown sources is also shown. **, P < 0.01.

FIG 6

Within and between pig farms dissimilarity measurements throughout the seasons. Shown are unweighted Jaccard (A) and weighted Ružička (B) distances in microbiota compositions within farms (pairwise distances between sample types originated from the same farm) and dissimilarities between farms (pairwise distances between samples originating from different farms). The lines represent the means and the shaded areas the 95% confidence intervals. *, P < 0.05; **, P < 0.01; ***, P < 0.001.