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The nasal microbiota of dairy farmers is more complex than oral microbiota, reflects occupational exposure, and provides competition for staphylococci.

ABSTRACT: Allergic and autoimmune diseases had been attributed to lack of exposure to biodiversity, an important factor in regulating immune homeostasis in a healthy host. We posit that the microbiome of healthy dairy farmers (DF) will be richer than non-farmers (NF) living in urban settings due to exposure to a greater biodiversity in the dairy environment. However, no studies have investigated the relationships between microbiota of dairy farmers (DF) compared with urban non-farmers (NF). We compared the nasal and oral microbiota of dairy farmers (N_DF, O_DF, respectively) with nasal and oral microbiota of NF in the same geographical area. The N_DF showed high microbial diversity with hundreds of unique genera that reflected environmental/occupational exposures. The nasal and oral microbiomes clustered separately from each other using Principal Coordinate Analysis, and with DF harboring two-fold and 1.5-fold greater exclusive genera in their nose and mouth respectively, than did non-farmers. Additionally, the N_DF group had a lower burden of Staphylococcus spp. suggesting a correlation between higher microbial diversity and competition for colonization by staphylococci. The N_DF samples were negative for the mecA gene, a marker of methicillin-resistance in staphylococci. The lower burden of staphylococci was found to be independent of the abundance of Corynebacterium spp. Exposure to greater biodiversity could enhance microbial competition, thereby reducing colonization with opportunistic pathogens. Future studies will analyze whether exposure to livestock microbiomes offers protection from acute and chronic diseases.

SUBMITTER: Shukla SK

PROVIDER: S-EPMC5574581 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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The nasal microbiota of dairy farmers is more complex than oral microbiota, reflects occupational exposure, and provides competition for staphylococci.

Shukla Sanjay K SK Ye Zhan Z Sandberg Scott S Reyes Iris I Fritsche Thomas R TR Keifer Matthew M

PloS one 20170829 8

Allergic and autoimmune diseases had been attributed to lack of exposure to biodiversity, an important factor in regulating immune homeostasis in a healthy host. We posit that the microbiome of healthy dairy farmers (DF) will be richer than non-farmers (NF) living in urban settings due to exposure to a greater biodiversity in the dairy environment. However, no studies have investigated the relationships between microbiota of dairy farmers (DF) compared with urban non-farmers (NF). We compared th ...[more]

PMID: 28850578

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Project description:Multiple epidemiological studies identify Dolosigranulum pigrum as a candidate beneficial bacterium based on its positive association with health, including negative associations with nasal/nasopharyngeal colonization by the pathogenic species Staphylococcus aureus and Streptococcus pneumoniae Using a multipronged approach to gain new insights into D. pigrum function, we observed phenotypic interactions and predictions of genomic capacity that support the idea of a role for microbe-microbe interactions involving D. pigrum in shaping the composition of human nasal microbiota. We identified in vivo community-level and in vitro phenotypic cooperation by specific nasal Corynebacterium species. Also, D. pigrum inhibited S. aureus growth in vitro, whereas robust inhibition of S. pneumoniae required both D. pigrum and a nasal Corynebacterium together. D. pigrum l-lactic acid production was insufficient to account for these inhibitions. Genomic analysis of 11 strains revealed that D. pigrum has a small genome (average 1.86 Mb) and multiple predicted auxotrophies consistent with D. pigrum relying on its human host and on cocolonizing bacteria for key nutrients. Further, the accessory genome of D. pigrum harbored a diverse repertoire of biosynthetic gene clusters, some of which may have a role in microbe-microbe interactions. These new insights into D. pigrum's functions advance the field from compositional analysis to genomic and phenotypic experimentation on a potentially beneficial bacterial resident of the human upper respiratory tract and lay the foundation for future animal and clinical experiments.IMPORTANCEStaphylococcus aureus and Streptococcus pneumoniae infections cause significant morbidity and mortality in humans. For both, nasal colonization is a risk factor for infection. Studies of nasal microbiota identify Dolosigranulum pigrum as a benign bacterium present when adults are free of S. aureus or when children are free of S. pneumoniae Here, we validated these in vivo associations with functional assays. We found that D. pigrum inhibited S. aureusin vitro and, together with a specific nasal Corynebacterium species, also inhibited S. pneumoniae Furthermore, genomic analysis of D. pigrum indicated that it must obtain key nutrients from other nasal bacteria or from humans. These phenotypic interactions support the idea of a role for microbe-microbe interactions in shaping the composition of human nasal microbiota and implicate D. pigrum as a mutualist of humans. These findings support the feasibility of future development of microbe-targeted interventions to reshape nasal microbiota composition to exclude S. aureus and/or S. pneumoniae.

Project description:Resources available in the human nasal cavity are limited. Therefore, to successfully colonize the nasal cavity, bacteria must compete for scarce nutrients. Competition may occur directly through interference (e.g., antibiotics) or indirectly by nutrient sequestration. To investigate the nature of nasal bacterial competition, we performed coculture inhibition assays between nasal Actinobacteria and Staphylococcus spp. We found that isolates of coagulase-negative staphylococci (CoNS) were sensitive to growth inhibition by Actinobacteria but that Staphylococcus aureus isolates were resistant to inhibition. Among Actinobacteria, we observed that Corynebacterium spp. were variable in their ability to inhibit CoNS. We sequenced the genomes of 10 Corynebacterium species isolates, including 3 Corynebacterium propinquum isolates that strongly inhibited CoNS and 7 other Corynebacterium species isolates that only weakly inhibited CoNS. Using a comparative genomics approach, we found that the C. propinquum genomes were enriched in genes for iron acquisition and harbored a biosynthetic gene cluster (BGC) for siderophore production, absent in the noninhibitory Corynebacterium species genomes. Using a chrome azurol S assay, we confirmed that C. propinquum produced siderophores. We demonstrated that iron supplementation rescued CoNS from inhibition by C. propinquum, suggesting that inhibition was due to iron restriction through siderophore production. Through comparative metabolomics and molecular networking, we identified the siderophore produced by C. propinquum as dehydroxynocardamine. Finally, we confirmed that the dehydroxynocardamine BGC is expressed in vivo by analyzing human nasal metatranscriptomes from the NIH Human Microbiome Project. Together, our results suggest that bacteria produce siderophores to compete for limited available iron in the nasal cavity and improve their fitness.IMPORTANCE Within the nasal cavity, interference competition through antimicrobial production is prevalent. For instance, nasal Staphylococcus species strains can inhibit the growth of other bacteria through the production of nonribosomal peptides and ribosomally synthesized and posttranslationally modified peptides. In contrast, bacteria engaging in exploitation competition modify the external environment to prevent competitors from growing, usually by hindering access to or depleting essential nutrients. As the nasal cavity is a nutrient-limited environment, we hypothesized that exploitation competition occurs in this system. We determined that Corynebacterium propinquum produces an iron-chelating siderophore, and this iron-sequestering molecule correlates with the ability to inhibit the growth of coagulase-negative staphylococci. Furthermore, we found that the genes required for siderophore production are expressed in vivo Thus, although siderophore production by bacteria is often considered a virulence trait, our work indicates that bacteria may produce siderophores to compete for limited iron in the human nasal cavity.

Project description:Background: There has been very little previous research in Ireland on the farmers' opinions regarding calf welfare issues. Calf welfare, particularly for male dairy calves, has assumed greater importance in Ireland in recent years due, in part, to an increase in the number of dairy cattle over the past decade. The objective of this study was to explore dairy farmers' views on a broad range of issues related to the expansion in the dairy herd. Methods: A survey was developed to capture the views of farmers regarding male dairy calves. The majority of questions were quantitative, and a final open-ended question collected qualitative data. The survey was distributed to ~2,900 dairy farmers via text message and 881 responses were received. Results: The sample was composed almost entirely of dairy farmers, although ~20% also had a beef enterprise on their farm. Fifty eight percent of the farmers were concerned with the increase in the number of male dairy calves in recent years. The EU's abolition of milk quotas, the profitability of dairy farming compared to other farm types, and guidance from farm advisors were the three highest ranked drivers behind the increase in the number of male dairy calves. The three highest ranked options for managing the number of male dairy calves were to increase exports, encourage greater use of sexed semen, and improve the beef merit of these calves. Eighty five percent of respondents stated that individual farmers had responsibility for making changes to the number of male dairy calves. The main themes arising from analysis of the responses to the open-ended question, seeking any additional comments, were breed, beef price, live exports, and sexed semen. Conclusions: Dairy farmers recognized the responsibility they have for making changes in respect of male dairy calves, and many demonstrated a willingness to make changes in this regard. The important role of other stakeholders, particularly suckler (system where reared from calf to beef) farmers, in rearing male dairy calves for beef production was also recognized. However, the issues of who bears the risks and costs associated with greater integration will have to be carefully considered.

Project description: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.

Project description:This study investigated 960 Slovak and Czech spotted cattle from four different conventional (non-organic) dairy herds located in Eastern Slovakia and Czechia during early lactation (14-100 days after calving). Dairy cows were examined clinically; milk from fore-stripping of each udder quarter was subjected to sensory examination and assessed by the California mastitis test (CMT), and laboratory analyses of bacterial pathogens in milk, including virulence factors, were conducted. Positive CMT scores (1-3) for one or more quarters were detected in 271 (28.2%) of the examined animals. Out of 230 infected milk samples, representing 24.0% of all dairy cows, staphylococci (59.1% of positive findings) were the most commonly isolated organisms, followed by E. coli (11.3%), streptococci Str. uberis (9.1%) and Str. agalactiae (3.4%), and enterococci (6.1%). From 136 isolates of S. aureus (38 isolates) and non-aureus staphylococci (NAS; 98 isolates), virulence factors and their resistance to 14 antimicrobials were detected using the disk diffusion method, with PCR detection of the methicillin resistance gene, mecA. An increased incidence of clinical and chronic forms of mastitis has been reported in mastitic cows in which staphylococci, especially S. aureus and NAS (S. chromogenes, S. warneri, and S. xylosus), have been detected and compared to other isolated udder pathogens. From those species, S. aureus and isolates of NAS mentioned above showed multiple virulence factors that are more likely to hydrolyze DNA, hemolysis, produce gelatinase and biofilm, and have multi-drug resistance as compared to other less virulent staphylococci. Generally, the isolated staphylococci showed 77.2% resistance to one or more antimicrobials, in particular to aminoglycosides, β-lactams, macrolides, or cephalosporins. Isolates that showed the ability to form a biofilm were more resistant to more than one antimicrobial than isolates without biofilm production. Multi-drug resistance to three or more antimicrobial classes was recorded in 16 isolates (11.7%), and the presence of the mecA gene was also confirmed in two isolates of S. aureus and two species of NAS.

Dataset Information

The nasal microbiota of dairy farmers is more complex than oral microbiota, reflects occupational exposure, and provides competition for staphylococci.

Publications

The nasal microbiota of dairy farmers is more complex than oral microbiota, reflects occupational exposure, and provides competition for staphylococci.

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