Bioaerosols and us
Each day, we inhale and ingest microscopic life: up to 60,000 fungal spores, 6 million bacteria, and the same for viruses. We also emit millions of biological particles from our bodies every day. Indeed, a person's mere presence in a room can add 37 million bacteria to the air through emission and displacement. We are also continuously exposed to other biological particles, such as pollen grains. Ancient Egyptians described these windblown packages that ensure the survival of flowering plants as ‘powder that gives life’. Between 2,500 and 20,000 pollen grains are inhaled by each of us daily. From this perspective, our bodies and surrounding environments are locked in a continuous biological exchange. Collectively, these airborne microorganisms and other biogenic compounds and particles are known as bioaerosols.
Historically, six dimensions have been included in bioaerosol research. These dimensions can be divided into the following three broad categories:
(i)
Earth systems – considers biogeography, the hydrological cycle, and atmospheric chemistry;
(ii)
Agriculture – focuses on bioaerosols and food production;
(iii)
Human health – primarily concerns allergenic particles and human pathogens.
Until recently, the focus of the third dimension (Human health) has been on understanding and controlling ‘unhealthy’ human exposures to airborne pathogens (i.e., disease-causing microorganisms), bacterial endotoxins, mycotoxins, and high-molecular-weight allergens (e.g., pollen).
Since the dawn of germ theory in the 1800s, microorganisms have largely been viewed as the bane of society, and humans have tried exhaustively to avoid exposure to them. After all, some microorganisms cause devastating diseases in humans, nonhuman animals, and plants. However, in recent years, our understanding of microbial ecology and microbiome science has deepened dramatically, and scientists now think that our reduced exposure to microbial biodiversity is linked to the rise in noncommunicable diseases (e.g., asthma and inflammatory bowel disease) and mental health conditions. Indeed, exposure to a diverse assemblage of environmental microorganisms plays a critical role in human health.
Most research on the benefits of diverse microbial exposures has focused on the diet (including breastfeeding) and the vaginal microbiome, as early exposure – during the weaning period – is considered a critical window to establish a ‘healthy’ gut microbiome. More recently, researchers have been testing the biodiversity hypothesis and how exposure to environmental microorganisms can change the human microbiome, leading to enhanced immune regulation and potentially other pathways to health. This paradigm shift in our understanding of the aerobiome (the microbiome of a given air space) appends a vital new dimension to bioaerosol research – health promotion via contact with beneficial microorganisms and plant-based compounds called phytoncides. These microbiota–host associations underpin a holistic view of health in which feedback loops between microbiota (including the aerobiome) and host are thought to maintain the health of our ‘walking ecosystems’.
The aerobiome–health axis
The aerobiome is the collection of microorganisms in an airspace, along with their cellular fragments and by-products of metabolism. The composition and function of the aerobiome can differ dramatically depending on environmental conditions. For instance, weather conditions, particularly air pressure and temperature, are known to drive daily fluctuations in aerobiome composition. The species richness of a local aerobiome can increase if the location is downwind from a biodiverse source (e.g., a forest). Moreover, the assembly of the aerobiome should be viewed from a three-dimensional perspective. A recent study showed that vertical stratification of the near-surface (biosphere) aerobiome occurs, with bacterial diversity decreasing with increasing height from the ground. This is perhaps unsurprising, as soil is one of the most biodiverse habitats on the planet. Yet it has important health implications, as it demonstrates that smaller people (e.g., children) and those who spend substantial amounts of time near the ground will inhale greater doses of microorganisms compared with taller people.
Land use (how the land is used) and land cover (the type of land covering a given surface) also dramatically influence the composition of the aerobiome. For instance, bacterial diversity is typically greater in urban areas with more complex vegetation than in monoculture habitats or grey infrastructure. Pollution also influences the aerobiome composition with important health implications. For example, deteriorating air quality can increase the proportion of airborne pathogens. Moreover, evidence suggests that air pollution can interact with the pollen grain microbiome and increase its allergenicity – with implications for inflammatory conditions. Artificial light and anthropogenic noise can also alter environmental microbiomes in ways that we do not yet fully understand. There is also an important temporal aspect to aerobiome assembly, with fluctuations in bacterial community structure occurring with time/season (e.g., diurnal cycles and seasonal fluctuations).
It is well known that airborne microorganisms and allergens can cause adverse impacts in humans, but what about the potential health benefits of exposure to the aerobiome? Emerging evidence demonstrates a link between aerobiome characteristics (e.g., its microbial diversity, abundance and/or functions) and immunological proxies that are consistent with a protective immune system effect. Exposure to urban house dust drives an allergic Th1-type immune response, while exposure to biodiverse rural dust drives a Th2-type anti-inflammatory immune response. This evidence (along with animal model studies) reinforces the notion that exposure to biodiverse aerobiomes can support healthy human immune function (i.e., characterised by fewer inflammatory and allergic responses). Evidence also suggests that exposure to phytoncides – compounds emitted by plants – can reduce blood pressure and enhance NK cell activity in people. Undoubtedly more research on the potential beneficial impacts of biodiverse aerobiomes on humans is needed. However, the limited evidence available does support the biodiversity hypothesis and the outcomes of other environmental microbiome studies demonstrating the immunomodulatory effects of interacting with biodiversity. For example, Roslund et al. (2021) showed that biodiversity interventions in day-care centres caused long-term shifts in commensal microorganisms in children and enhanced immune function.
Harnessing the aerobiome for improved health
Understanding the various environmental and social factors that shape the composition of the aerobiome, and the health impacts of exposure to the aerobiome, paves the way for landscape architects, town planners and restoration ecologists to develop interventions that promote human health via this pathway. Soil health is likely to be a vital factor in keeping the aerobiome biodiverse and in a health-promoting state, as the aerobiome is largely of soil origin. The potential for landscape managers to restore soil biodiversity to promote a healthy aerobiome reflects an important yet understudied facet of urban ecosystem health. Moreover, knowing that vegetation complexity could increase the health-promoting quality of the aerobiome means that landscape interventions can be designed to influence vegetation and management schemes with human health in mind. This aerobiome–landscape–human health nexus also adds to the recent calls to recognise ecosystem restoration as a public health intervention. The EcoHealth, One Health, and Planetary Health philosophical frameworks all recognise that human health is intimately dependent on healthy ecosystems. Local and global policy developments focusing on ecosystem restoration are needed to integrate frameworks that encourage health–biodiversity co-benefits in our everyday lives. The health-promoting (along with demoting) capacity of the aerobiome requires more research and attention as it provides landscape architects and ecologists with immense potential to positively shape the health of people and ecosystems.
Aerobiome policy needs
More research into the health-promoting properties of the aerobiome (and how we can influence these) is needed to inform policy developments and to provide evidence-based tools to inform guidelines and catalyse cross-sectoral policy processes. However, current evidence indicates that we know enough to act now with regard to restoring and creating healthy environments to promote human health via the aerobiome. Examples of relevant, broad-scale, international policies include the Sustainable Development Goals (particularly goals 3 – Good Health and Wellbeing, 11 – Sustainable Cities and Communities, and 15 – Life on Land), the Conferences of the Parties to the UN Framework Convention on Climate Change (UNFCCC), and the Convention on Biological Diversity, and the World Health Assembly. Moreover, initiatives need to be developed to support this paradigm shift in thinking about bioaerosols. One recent example is the UK Research and Innovation (UKRI) Clean Air Programme funded BioAirNet network (https://bioairnet.co.uk/).
Future bioaerosol initiatives aimed at integrating aerobiome knowledge to improve human and ecosystem health must recognise that there is currently no common conception of biologically ‘healthy’ air. This is a barrier to policy development and discourse with stakeholders who have the power to shape aerobiome exposures. Such initiatives should:
(i)
Bring together international academics and practitioners to advocate for building a balanced view of the aerobiome (and other aspects of bioaerosols), including both the health-demoting (pathogenic microorganisms and allergens) and promoting (beneficial microorganisms and biogenic compounds) elements. This will align with the healthy ecosystem, healthy people paradigm and with the policy frameworks listed above.
(ii)
Work to stimulate policy developments whilst acknowledging that there are many bioaerosol unknowns, that ‘healthy air’ has several interacting components spanning biological and social realms, but that a balanced view of the aerobiome is required that moves away from the focus on its pathogenic potential.
(iii)
Better understand, through empirical research, the health-promoting potential of the aerobiome and how we can shape it through landscape interventions. Developing this knowledge and associated policies will provide an immense opportunity to enhance ecosystem health.