Unifying Atmospheric Biology Research for the US Scientific Community

Communications

Unifying atmospheric biology research for the U.S. scientiﬁc community

1,3 2 CLAIRE G. WILLIAMS AND DAVID J. S MITH

1Department of Environmental Sciences, American University, Washington, D.C. 20016 USA 2Space Biosciences Research Branch, NASA Ames Research Center, Moffett Field, California 94035 USA

Citation: Williams, C. G., and D. J. Smith. 2021. Unifying atmospheric biology research for the U.S. scientific community. Ecological Applications 31(3):e02275. 10.1002/eap.2275

Abstract. A global COVID-19 pandemic, rising asthma and allergies, along with climate change impacting storm intensity and frequency, point to an urgent need to unify U.S. atmospheric biology research. To this end, we briefly define atmospheric biology, summarize its fragmented history, and then outline how to unify the field to provide benefits for the U.S. science community and its citizens. Atmospheric biology refers to the study of concentrations, sources, sinks, transformation, and impacts of airborne microorganisms inclusive of pollen, fungal spores, algae, lichens, bacteria, viruses, cellulose fibers, and other biomolecules or frag- ments of cells. Here our focus is biological particles, both respirable (PM10) and systemic (PM2.5). Due to its interdisciplinary dependencies and broadness of scales from nanometers to kilometers, atmospheric biology research is highly fragmented in the U.S. science community. It lacks shared paradigms and common vocabulary. This deficit calls for recognizing atmospheric biology as a research community in its own right, thereby linking human health to climate change. We need to recognize atmospheric biology’s importance to national security and science diplomacy. Advanced atmospheric biology research is being conducted in Europe, Rus- sia, and China, not in the United States. Key words: aerial biota; aerobiology; bioaerosols; COVID-19; pollen; primary biological aerosol particles; Valley Fever.

2015), depositing contagion, allergens, and pollutants INTRODUCTION inside closed spaces whether residential, ocean shipping, Bioaerosols compose 5% to 50% of atmospheric aero- aviation, or aerospace (Gregory 1961, Hammond et al. sols and its largest emitters are cities, forests, and deserts 1989, Osman et al. 2008, Yang et al. 2011). Consider that (Fig. 1; Frohlich-Nowoisky€ et al. 2016, Santl-Temkiv^ the U.S. Atlantic Seaboard alone exports pollen, spores, et al. 2020). Related terminology, as indicated by a Web sea salt, and combustion engine pollutants while import- of Science search, includes bioaerosols (n = 737), air- ing volcanic ash from Iceland and dust from the Sahara borne life (n = 569), aerobiology (n = 235), or airborne Desert (i.e., Mohanty et al. 2017, Flower and Kahn organisms (n = 199). Whether traced by aircraft, alpine 2020, Kramer et al. 2020). Outside of North America, observatories, or stationary tall towers such as WLEF, transboundary transport of bioaerosols is well docu- ATTO, and ZOTTO (e.g., Jaenicke 2005, Smith et al. mented (i.e., Schweitzer et al. 2018, Soleimani et al. 2013, Mikhailov et al. 2017, Figs. 2 and 3), we now 2020), thus we assert that bioaerosols are a globally know bioaerosols can be scattered by global circulating shared commons. winds and thus subject to long-range intercontinental transport (Smith et al. 2013, Tellier et al. 2019). This BIOAEROSOLS AS A GLOBALLY SHARED COMMONS means that atmospheric aerosols and their biotic load flow across national borders (Smith 2013, Yang et al. Bioaerosols not only physically connect nations but also scientifically connect disciplines. Collaboration is essential. Observing emissions, long-range transport, Manuscript received 16 August 2020; revised 14 November and deposition of bioaerosols require many types of sci- 2020; accepted 24 November 2020. Corresponding Editor: David S. Schimel. entific expertise. Instead of collaboration, U.S. research 3 E-mail: [email protected] on bioaerosols is minimal, sparse, and as disconnected

Article e02275; page 1 Ecological Applications Article e02275; page 2 CLAIRE G. WILLIAMS AND DAVID J. SMITH Vol. 31, No. 3

FIG. 1. Demonstrating the scale of atmospheric biology from micrometers to kilometers. (A) Saharan dust plume leaving Africa and traveling across the Atlantic Ocean to the United States in June 2020, as observed by NASA satellites. (B) Examples of bacteria commonly dispersed in the atmosphere. Image credits: NASA. ommunications C

FIG. 2. ZOTTO tall tower observatory and its surrounding forests in central Siberia. Photo credit: Anastasia Makhnykina, Sukachev Institute of Forest, Krasnoyarsk, Russia. April 2021 ATMOSPHERIC BIOLOGY Article e02275; page 3 C ommunications

FIG. 3. Sampling bioaerosols using C-20A aircraft above the U.S. Sierra Nevada Mountains Photo credit: NASA. from other scientific disciplines as it is from national biomedical research requires atmospheric biology as science policy. its unifying theme. Atmospheric biology is best seen as a unifying theme. It requires study at scalar extremes, spanning NEEDED: UNIFIED ATMOSPHERIC BIOLOGY FOR INTERNA- 14 orders of magnitude (Williams and Despres 2017) TIONAL COLLABORATION AND SCIENCE DIPLOMACY and methods resolution is still improving at either of its scalar extremes (e.g., Omar et al. 2009, Frohlich-€ Atmospheric biology research has been well sup- Nowoisky et al. 2016). Birch pollen neatly illustrates ported in western Europe and the Soviet Union. A this point. The major birch pollen allergen protein reunified Germany later strengthened its post-Soviet Bet v1 is characterized by molecular isoforms (e.g., scientific investment, inclusive of atmospheric biology. Spiric et al. 2015, von Loetzen 2019) yet satellite China has risen to become a major contributor. While LiDAR is required to observe dense concentrations of Europe, Russia, and China now recognize the value birch pollen at 2–3 km above the earth’s surface (e.g., of atmospheric biology to national security (Shen and Sassen 2008, Omar et al. 2009). Such weather-induced Yao 2013, Frohlich-Nowoisky€ et al. 2016, Haddrell Ecological Applications Article e02275; page 4 CLAIRE G. WILLIAMS AND DAVID J. SMITH Vol. 31, No. 3

and Thomas 2017), this is not the case for the United National Oceanic and Atmospheric Administration States. Not only do we have little recognition of its (NOAA) supports field campaigns, sometimes in coordi- role in national security, federal funding chances for nation from NASA representing a rare example of inter- U.S.-based atmospheric biology research is dismal agency cooperation in atmospheric biology. even though we are living in the age of pandemics. Disturbingly, as we are learning from the COVID-19 Valley Fever outbreak as an example crisis, U.S. atmospheric biology is indisputably too small, too isolated, and too fragmented. Consider the The challenge of studying Valley Fever outbreaks in state of our national portfolio (Table 1). The National the western United States, caused by aerosolized Coccid- Institutes of Health (NIH) has one institute for lung ioides spp. fungal spores, illustrates how the complexity research and yet another for immunology and infectious of scales within the atmospheric biology problem can diseases. The National Science Foundation (NSF) has only be addressed through coordination across federal funded investigations characterizing the relationship entities. Outdoor bioaerosol transmission of fungal between atmospheric microorganisms and precipitation. spores, pollen and even virus particles can be transconti- Similarly the Department of Energy (DOE) has sup- nental (Gregory 1961, Hammond et al. 1989). But ported small-scale atmospheric genomics. The U.S. whether this type of bioaerosol remains infectious out- Department of Agriculture (USDA) is responsible for doors depends on land use, meteorology and human risk monitoring airborne pathogens that threaten food sup- factors (Poulson et al. 2016, Schweitzer et al. 2018, Solei- ply as well as long-distance pollen flow between domesti- mani et al. 2020). Imagine if the next major Valley Fever cated crops and their wild relatives. Responsibility for outbreak occurred while federal roles outlined in Table 1 human health and epidemiological surveys of airborne were in place. Perhaps the same domestic network, had pathogens falls primarily under the Center for Disease it been realized prior to the COVID-19 pandemic, would Control (CDC). At the same time, the Department of have been a rapid resource for contact tracing and Defense (DOD) has oversight of biological warfare resolving the question of aerosol transmission. agents (e.g., anthrax dispersal) and other real-time national security monitoring assets. The U.S. Geological PROPOSING A NEW PROFESSIONAL ASSOCIATION FOR U.S. Survey studies bioaerosols in global desert dust (i.e., ATMOSPHERIC BIOLOGY Soleimani et al. 2020). The National Aeronautics and Space Administration (NASA) measures particulates Where to go from here? We can start by forming a using various satellites, modeling tools, and aircraft. new professional association for atmospheric biology. NASA also makes large-scale observations, predictions While we do recognize the laudable efforts of the Pan- and measurements of aerosol dispersal, including atmo- American Aerobiology Association and the Interna- spheric microorganisms (i.e., Smith et al. 2018). The tional Aerobiological Association, we still see the need for a different kind of U.S.-based professional association. Its focus would be on the research–policy interface, acting to aggregate research across relevant disciplines, TABLE 1. An idealized national framework for investigating Valley Fever in the western United States. perhaps similar to the European Aerobiology Society. ommunications To our thinking, this new professional association would Federal agency Potential role do the following: (1) provide best available science to

C U.S. Department of land use data sharing and policymakers, (2) identify and bridge research gaps, (3) Agriculture (USDA) monitoring stations cross-educate atmospheric scientists and biomedical Center for Disease Control public health surveys and risk experts together, (4) build science diplomacy dialogue, (CDC), National Institutes factor analysis and (5) engage through citizen science. of Health (NIH) As a first step, we ask the Ecological Society of Amer- U.S. Geological Survey geochemical and biological (USGS) characterization of aerosols, ica (ESA), as publisher of Ecological Applications,to bioaerosols work with us on proposing a Gordon Conference for National Aeronautics and high-altitude, long-duration Atmospheric Biology. Equally valuable are ESA-led Space Administration aircraft and field workshops for biomedical-meteorology cross-training. (NASA), National Science observatories; research Foundation (NSF) coordination networks and This could catalyze new curricula and courses for uni- FFRDCs (e.g., UCAR, versity students and professionals. Also, given the global NCAR) nature of atmospheric biology and the massive scales Department of Energy predictive modeling required for acquiring samples, we anticipate a role for (DOE), National Oceanic and Atmospheric citizen scientists to help provide samples and data of Administration (NOAA) annual precipitation entrapping bioaerosols. This type Department of Defense risk mitigation (e.g., personal of citizen science has been successful in a related endea- (DOD) protective equipment for vor, the U.S.A. National Phenology Network (Betan- vulnerable populations) court et al. 2011). Formalizing joint research and scientific diplomacy with Russia, China, Canada and the April 2021 ATMOSPHERIC BIOLOGY Article e02275; page 5

European Union would link U.S. atmospheric biology Mohanty, R. P., M. A. Buchhaim, J. Anderson, and E. Levetin. to national security issues and international relations. 2017. Molecular analysis confirms the long-distance transport of Juniperus ashei pollen. PLoS One 12:e0173465. Morris, C. E., et al. 2008. The life history of the plant pathogen CONCLUSIONS Pseudomonas syringae is linked to the water cycle. ISME Journal 2:321–334. There is no doubt that U.S. atmospheric biology has Omar, A., et al. 2009. The CALIPSO automated aerosol classi- been overlooked as a field of inquiry for over a half-cen- fication and LiDAR ratio selection algorithm. Journal of tury (Gislen 1948). To remedy this, we need a swift call Atmospheric & Oceanic Technology 26:1994–2014. to action, perhaps seen as a lasting nod to the COVID- Osman, S., et al. 2008. Microbial burden and diversity of com- 19 pandemic. So let us collect a national atmospheric mercial airline cabin air during short and long duration of travel. ISME Journal 2:482–497. biology portfolio then unify it with a new kind of profes- Poulson, R. L., et al. 2016. Environmental stability of swine and sional association. We require science diplomacy for human pandemic influenza viruses in water under variable working with bioaerosols as a shared global commons conditions of temperature, salinity and pH. Applied and and this can bridge better collaboration, on both regio- Environmental Microbiology 82:3721–3726. nal and intercontinental scales, as we seek to learn more Santl-Temkiv, T., et al. 2020. Bioaerosol field measurements: about how bioaerosols impact our lives. We owe future challenges and perspectives in outdoor studies. Aerosol Science and Technology 54:520–546. generations something more than an unseen wilderness Sassen, K. 2008. Boreal tree pollen sensed by polarization lidar: between the gutter and the stars (Wilde 1917). depolarizing biogenic chaff. Geophysical Research Letters 35: C L18810. ACKNOWLEDGMENTS Schweitzer, M. D. 2018. Lung health in era of climate change

and dust storms. Environmental Research 163:36–42. ommunications Special thanks to the constructive ideas of David Schimel at Shen, F., and M. Yao. 2013. Are we biologically safe with snow NASA-JPL and to the Russian National Academy of Sciences precipitation? A case study in Beijing. PLoS One 8:e65249. for its hospitality at the Sukachev Institute of Forest and Smith, D. J. 2013. Aeroplankton and the need for a global mon- ZOTTO tall tower observatory in Zotino, Krasnoyarsk Krai, itoring network. BioScience 63:515–516. Russian Federation. Atmospheric biology research was sup- Smith, D. J., et al. 2013. Intercontinental dispersal of bacteria ported by the Fulbright Program of Russia (C. G. Williams). and archaea by transpacific winds. Applied and Environment Microbiology 79:1134. Smith, D. J., et al. 2018. Airborne bacteria in earth’s lower LITERATURE CITED stratosphere resemble taxa detected in the troposphere: Betancourt, J. L., et al. 2011. Implementing a U.S. national phe- results from a new NASA aircraft bioaerosol collector. Fron- nology network. Eos, Transactions American Geophysical tiers in Microbiology 9:1752. Union 86:539. Soleimani, Z., et al. 2020. An overview of bioaerosol load and Flower, V. J. B., and R. A. Kahn. 2020. The evolution of Ice- health impacts associated with dust storms: a focus on the landic volcano emissions as observed from space in the era of Middle East. Atmospheric Environment 223:117184. NASA’s earth observing system (EOS). Journal of Geophysi- Spiric, J., A. M. Engin, M. Karas, and A. Reuter. 2015. Quality cal Research: Atmospheres 125:e2019JD031625. control of biomedical allergen products—highly complex isoal- Frohlich-Nowoisky,€ J., et al. 2016. Bioaerosols in the Earth sys- lergen composition challenges standard MS database search tem: climate, health and ecosystem interactions. Atmospheric and requires manual data analyses. PLoS One 10:e0142404. Research 182:346–376. Tellier, R., Y. Li, B. J. Cowling, and J. W. Tang. 2019. Recogni- Gislen, T. 1948. Aerial plankton and its conditions of life. Bio- tion of aerosol transmission of infectious agents: a commen- logical Reviews of the Cambridge Philosophical Society tary. BMC Infectious Diseases 19:101–110. 23:109–126. von Loetzen, C., et al. 2019. Quality and potency profile of Gregory, P. H. 1961. The microbiology of the atmosphere, eight recombinant isoallergens largely mimicking total Bet London: Leonard Hill Ltd. v1-specific IgE binding of birch pollen. Clinical and Experi- Haddrell, A. E., and R. J. Thomas. 2017. Aerobiology: experi- mental Allergy 49:712–723. mental considerations, observations and future tools. Applied Wilde, O. 1917. Lady Windermere’s fan. https://www.gutenbe and Environment Microbiology 83:e00808–e817. rg.org/files/790/790-h/790-h.htm Hammond, G. W., R. L. Raddatz, and D. E. Gelskey. 1989. Williams, C. G., and V. R. Despres. 2017. Temperate and boreal Impact of atmospheric dispersion and transport of viral aero- forests are a substantial pollen contributor to seasonal bio- sols on the epidemiology of influenza. Reviews of Infectious genic emissions. Forest Ecology and Management 401:187– Diseases 11:494–497. 191. Jaenicke, R. 2005. Abundance of cellular material and proteins Yang, Q., et al. 2015. Aerosol transport and wet scavenging in in the atmosphere. Science 308:73. deep convective clouds: a case study and model evaluation Kramer, S. J., et al. 2020. Subseasonal variability of elevated using a multiple passive tracer analysis approach. Journal of dust concentrations over South Florida. Journal of Geophysi- Geophysical Research Atmospheres 120:8448–8468. cal Research: Atmospheres 125:e2019JD031874. Yang, W., S. Elankumaran, and L. C. Marr. 2011. Concentra- Mikhailov, E., et al. 2017. Long-term measurements (2010– tion and size distributions of airborne influenza A viruses 2014) of carbonaceous aerosols and carbon monoxide at the measured indoors at a health centre, a day-care centre and on Zotino Tall Tower Observatory (ZOTTO) in central Siberia. aeroplanes. Journal of the Royal Society, Interface 8:1176– Atmospheric Chemistry and Physics 17:14365–14392. 1184.