We have been focusing on a pathogenic virus for several years and may have forgotten that most microbes, meaning bacteria, viruses, and fungi, actually benefit humankind. In fact, we depend on trillions of microbes that reside in and on our body — our microbiome — for our very survival. Food digestion, immune system training, blood clotting, and prevention of invasive infections are just a few of the human physiologic functions that require the help of microbes.

Surprisingly, a given species of bacteria or virus is not binarily good or bad (with a few exceptions) but function along a spectrum ranging from harmful, pathogenic (Greek: the birth of pain) to helpful, or commensurable (Latin: to eat from the same table) strains. The gradation of microbial interactions with humans, from helpful to disease-causing, are driven by both environmental selection pressures and by variations in the robustness of the human host immune system.

As auto-immune diseases, allergic disorders, and other illnesses rise in developed countries, perturbations in the human microbiome are being examined. One of the factors identified as a driving force that shapes the human microbiome is the indoor environment, where we spend the vast majority of our time.

This column explores the relationships between pathogenic or commensural microbes that comprise the indoor microbiome, IAQ, and the human immune system.

How Do Good Microbes Move to the Dark Side?

No single gene makes a microorganism a pathogen, and no clear-cut cell characteristics separate a pathogen from a non-pathogen. Rather, microbes have the ability to quickly adapt to changing environmental conditions to ensure their survival. Recognition of an organism as a pathogen is not always simple, however, in the biological sense, pathogens possess the ability to cross anatomic barriers or breach other host defenses that limit the survival or replication of other microorganisms. When host defense mechanisms that suppress pathogen entry, attachment, invasion, and replication to prevent allergies or infection are breached, disease occurs. If microbial adaptations include a shift from helpful to harmful, we humans should not take this personally but should understand and manage the forces which drive the change.

One general principle of biology that clearly applies to the indoor microbiome is that more diverse indoor microbial communities have fewer pathogenic strains, similar to a healthy garden. Conversely, less microbial diversity is associated with more pathogenic strains.

The next question to grapple with is what environmental factors are associated with changes in building microbiome diversity and the expression of pathogenic states? The microbial cell (focusing on bacteria) membrane detects subtle changes in temperature, vapor pressure, oxygen partial pressure, pH, and metal ion concentrations in their mileux and, if necessary for survival, signals to intracellular organelles to mobilize previously unexpressed virulence traits. For example, reversible expression of virulence genes by extreme temperatures or low water vapor is common to many pathogens. Microbes, remaining dormant for long periods in extreme temperatures or anhydrous conditions, mobilize virulence-specific genes when returned to a warm and moist mammalian body.

Another survival tactic that convers increased pathogenecity is the intimate sharing of genes that convey antimicrobial resistance. The promiscuous transfer of virulance traits, called horizontal gene transfer, occurs frequently and rapidly in bacterial communities threatened by extinction. Enterococcus faecium is an example of a nonpathogenic bacterial strain evolving harmful virulence via horizontal gene transfer. This initially commensal bacterium acquired new genetic elements driven by environmental selection pressures in intensive care units, rapidly evolving into a virulent pathogen with high morbidity rates in infected hospitalized patients.

What We Know About IAQ Influences

The multitude of good microbes in and on each of us form a line of defense on our skin and in our respiratory tracts, intestines, and vaginas (if you have one) that protects us from invasion by pathogenic microbes. By competing for nutrients, secreting chemicals, and other strategies, microbes, paradoxically, keep infectious pathogens in check. This balance is disrupted when, for example, we take antibiotics. It is also disrupted when an environmental trigger either reduces the function of our immune system or increases the virulence of a specific microbe. Our microbiome plays a role in these activities by modulating the structure and function of the epithelial barriers.

This equilibrium is challenged by exposure to air pollutants. For example, inhalation of carbon combustion byproducts from traffic or other sources reduce protective microbiota and increase the presence of potential pathogens in the upper airways. Another example is that the proportions of pathogenic bacteria in air with high levels of PM2.5 and PM10 are increased, showing that pathogenic bacteria can endure more air toxins than commensural bacteria. In short, when air pollutants are present, more pathogenic bacteria survive as good bacteria die. These pathogen virulence increases add to other harmful effects of air pollution on lungs and cardiovascular systems.

Clearly, building managers are in a good position to support occupant health by managing IAQ to boost good microbes and diminish pathogenic ones.

Steps to Managing IAQ to Support Diverse, Healthy Microbiomes

1. Understand that indoor temperature, humidity, airflow rates, carbon dioxide levels, particles, and chemicals can create survival pressures for specific microbial taxa;
2. Use natural ventilation, when possible, to introduce diverse, outdoor airborne bacterial communities;
3. Ventilate with appropriate air exchange rates and directional airflow to reduce the concentrations of airborne microbial pathogens;
4. Avoid excessively high, energy-consuming ventilation rates that cause turbulence, which retains particulates and potentially pathogenic microbes in the breathing zone;
5. Maintain ventilation systems properly to prevent amplification and spread of pathogens;
6. Replace degrading building materials that could provide substrates and nutrients for pathogens;
7. Keep indoor relative humidity (RH) in the healthy midrange of 40%-60%. Low RH (below 40%) increases the aerosolization and resuspension of microorganisms from the floor and high-touch surfaces, increasing the potential for infectious aerosols to stay in the breathing zone of occupants longer and travel farther to infect secondary hosts. RH over 60% is conducive to microbial survival surfaces, facilitating direct contact transfer of pathogens to occupants;
8. Stop trying to eradicate all microorganisms from indoor air and surfaces. Avoid excessively strong, antimicrobial chemicals in surface cleaning. These impose selective pressures that increase the risk of producing resistance strains as well as indiscriminate killing of beneficial microorganisms, which allows overtaking by pathogenic organisms;
9. Avoid disinfecting chemicals that can introduce volatile organic compounds and secondary aerosols that create exposure risks to occupant airways and skin;
10. Get a dog. Exposure to diverse microbiomes from dogs early in life has been associated with reduced rates of asthma and infections.

Microbes have co-evolved with us, playing crucial supporting roles in our physiology, immunity, and metabolism. Maintaining IAQ to support beneficial microbes and diminish the presence of pathogenic ones provides each of us with the powerful, personalized medicine of a healthy microbiome.