This study examined differences in household characteristics, environmental factors, socio-economic factors, and microbial composition of dust from households in neighborhoods across the US-MX Border, in which we previously documented differential rates of asthma prevalence [29]. We identified multiple structural, environmental, and human factor differences between the US and MX homes, which may have led to the differences seen in dust loading and microbial diversity across the dust samples collected from the homes. The bacterial genera A. Alishewanella and Chryseomicrobium were found to be enriched in the dust from homes within MX, while Geodermatophilus was found to be enriched in the dust from homes within the US.
This study found multiple housing characteristics that differed between MX and the US, differences that may contribute to the higher prevalence of asthma in children of Mexican descent living in the US compared to MX [29]. Homes in the US were more likely to be on paved roads and to have flushing toilets, piped/municipal water, more rooms and bathrooms, and evaporative cooling and/or air conditioning compared to MX homes. Although only 26.3% of individuals in the US drank their tap water, this was significantly higher than in MX (2.6%). It has been shown that municipal water has fewer commensal microbes present and that drinking of municipal water is associated with higher prevalence of asthma and allergies [21, 30]. Floors were more likely to be carpeted in the rooms where the dust was collected in the US. Carpets in the home may be an important risk for asthma development as they can be a reservoir for mildew, mold, allergens, and chemical hazards (e.g., pesticides, metals, flame retardants, per-and polyfluoroalkyl substances (PFAS), and can contribute to poor indoor air quality [31, 32]. Although carpets typically have greater dust loading than hard floors, the homes in MX had significantly greater dust loading than the ones in the US, despite the lack of carpet (Tables 2 and 3). This suggests that differences in the household density (particularly the number of children), the presence of pets, and other household structural factors between these communities might account for the greater dust loading in MX.
Microbial populations in indoor environments, where we live and eat, play an important role in human health. Environmental dust exposure early in life appears to influence what bacteria colonize the gut, skin, and nasal microbiome [33–36]. It has been proposed that part of the reason for increasing asthma and allergy prevalence worldwide is due to shifts in our lifestyles towards more Western or Modernized ways of living, which has led to a decrease in microbial exposure during a critical period of immune development [37]. Individuals with exposure to more diverse bacteria have lower rates of allergic diseases [38, 39]. We found significant differences in the microbiome composition of dust collected from homes in MX compared to the US (Fig. 1). Previous studies have shown a link between house dust microbial composition and risk of allergic asthma development. Children raised in Amish communities have lower rates of allergic sensitization and asthma than those from Hutterite communities. Stein et al demonstrated that house dust from an Amish community had a different microbial composition than the house dust from a Hutterite community. Further, mice that received the dust from the Hutterite houses intranasally had decreased airway reactivity and eosinophilia, which are markers of allergic asthma [22]. There was no difference in microbial dust composition between homes with and without an occupant that reports having asthma. There are likely multiple reasons for this finding. First, the study was not powered to find a difference based on asthma prevalence, and the study simply asked if a person in the household had asthma and not whether they grew up in that house. Also, the study did not use a validated tool to screen for asthma in all household occupants, so there may be a difference in asthma detection between the cities.
House dust microbial composition is affected by outdoor and indoor environments, including structural characteristics, as well as household occupants and their activities in the home. Any combination of the significant differences between the homes in MX and the US may have led to the differences observed in the microbial composition of the house dust. A sub-analysis showed that there was a difference in beta diversity (unweighted UniFrac) of the dust microbiome when comparing the homes by road type and presence of air conditioning. Using an air conditioner changes the indoor environment by changing the temperature and humidity, which would lead to differences in microbial growth indoors [40], as well as through filtering of the air. Homes with air conditioners are less likely to have windows open, and therefore less dust is likely to blow into the home. Furthermore, it has been shown that as regions become more industrialized and homes are constructed in a manner where they are more tightly sealed, the microbiome diversity decreases [41]. The structural differences and occupant behavioral differences between US and MX are likely to have led to the differences in microbial diversity in the household dust.
We have previously shown that these two regions have different prevalence of childhood asthma, and this study also found differences in house dust composition between the two regions. The dust from the US homes was more enriched with the genus Geodermatophilus, whereas the dust from Mexican homes was more enriched with A Alishewanella and Chryseomicrobium. While the genera of bacteria found in house dust in both the US and MX have not been previously identified as related to asthma prevalence, Ornithinimicrobium (more abundant in the low SES NMX neighborhood) and Geodermatophilus are part of the phylum Actinobacteria, which has been shown to be both negatively and positively associated with allergic disease [25, 42–46]. To our knowledge, Geodermatophilus has not been specifically linked to being a risk for asthma development previously, but its presence in school dust has been linked to “Sick Building Syndrome” [47]. The genus Alishwaneela is a gram-negative species that have endotoxin present in their cell walls. Previous studies have shown that higher levels of endotoxin in a child's environment are related to lower incidence of atopic asthma and allergic diseases [22, 48, 49]. Alishwenella is also in the phylum of Proteobacteria, which, much like Actinobacteria, has been shown to be both negatively and positively associated with allergic disease in different studies [42, 43, 46, 50]. Chryseomicrobium is in the family Planococcaceae. In a study by Ta et al. it was shown that Pamnomicrobium, which is also in the family Planococcaceae, was protective against developing allergic eczema [44]. The inconsistencies in the direction of these relationships may be explained by the need to classify beyond the phylum level, which is very broad, or the presence of critical time points at which exposure protects against onset of asthma but may be harmful once asthma has developed. In any case, the differences found in microbial exposure between the sites suggest promising areas for future research related to asthma in the Border region.
Although some microbes in the dust are unlikely to be active metabolically, others are living and metabolically active, and so may play a critical role in alteration of host microbiome. They can colonize the host, where they can become metabolically active and play a key role in risk of asthma development. A PICRUSt analysis was done to identify potentially relevant metabolic pathways present in the house dust from homes located in MX vs US. There were 23 biosynthetic pathways, 38 degradation/utilization/assimilation pathways, and 7 pathways involved in generation of precursor metabolites that were higher in the house dust from MX. Some of the pathways found to be more prevalent in the house dust from MX are involved in biosynthesis of molecules that are known to be protective against asthma (Supplemental Fig. S4), such as short chain fatty acids and pyrimidine [51, 52]. There have been multiple studies that show the importance of metabolites produced by the microbiota that colonize humans in protecting against asthma via alterations in the epithelial barrier function and immune system regulations. Many of the possibly up-regulated functional pathways present in the house dust from MX have been examined in other studies and have been shown to be protective against asthma or helpful in asthma control. For example, the UDP − N−acetyl − D−glucosamine and the mycolate biosynthetic pathways that were higher in the house dust from MX have been shown to down-regulate allergic airway inflammation [53–56] (Supplemental Fig. S4).
Limitations of this study include that collection of the house dust microbiome samples occurred at a single time-point and during a single season. There was significant differences in the ambient temperatures during sample collection across the border and this was likely related to more of the MX samples being collected in the spring/summer months and more of the US sample being collected in the winter. Future studies would benefit by looking at multiple time points to assess the variability of household microbiomes. The high SES NMX homes were all part of a subdivision with identical floor plans, which could drive some of the differences observed between the low and high SES neighborhoods in NMX. We used 16S rRNA amplicon sequencing to characterize the house dust, which generally supports taxonomic resolution only at approximately the genus level, although species level differences may affect human health. Shallow or deep shotgun metagenomics, although more expensive, would improve microbial identification, and deep shotgun metagenomics would provide more accurate functional profiles of the samples. PICRUSt uses 16S rRNA data to extrapolate metagenome composition and provides relatively lower confidence functional pathway profiles of samples. Given that asthma is a common reason for presentation to outpatient clinics and household recruitment was through outpatient clinics, there may have been selection bias because families that had an asthmatic child in the home may have been more likely to enroll in the study. However, this bias could have been represented on both sides of the Border. We did not investigate differences in pollutants in the collected dust, such as metals or pesticides, which could affect the dust composition and microbial diversity, along with the growth of opportunistic bacterial pathogens [57].
In conclusion, despite TUS, NUS, and NMX being geographically close (< 100 km) and having similar climates, homes across this Border region differ in ways that lead to significantly different indoor environments. Mexican and US households differed in years of education; household income; the percentage of homes that had paved roads, flushing toilets, and piped water; the number rooms and bathrooms present in the home; and presence and type of cooling and flooring. Some of these household differences may have led to the significant differences we observed in the microbial composition of the house dust collected from MX or US homes. The dust from the US homes was more enriched with the genus Geodermatophilus, whereas the dust from Mexican homes was enriched with A. alishewanella and Chryseomicrobium. Future research should assess whether exposure to these bacteria during critical windows in early life may offer protection from development of asthma or allergic disease.