Bioaerosols in the Earth system: Climate, health, and ecosystem interactions

Highlights

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  Aerosols of biological origin play a vital role in the Earth system.

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  Bioaerosols are essential for biological reproduction and can cause diseases.

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  Bioparticles can serve as nuclei for cloud droplets, ice crystals, and precipitation.

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  Interaction and co-evolution of life and climate in the Earth system

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  Overview of the state of bioaerosol research and recent advances

Abstract

Aerosols of biological origin play a vital role in the Earth system, particularly in the interactions between atmosphere, biosphere, climate, and public health. Airborne bacteria, fungal spores, pollen, and other bioparticles are essential for the reproduction and spread of organisms across various ecosystems, and they can cause or enhance human, animal, and plant diseases. Moreover, they can serve as nuclei for cloud droplets, ice crystals, and precipitation, thus influencing the hydrological cycle and climate. The sources, abundance, composition, and effects of biological aerosols and the atmospheric microbiome are, however, not yet well characterized and constitute a large gap in the scientific understanding of the interaction and co-evolution of life and climate in the Earth system. This review presents an overview of the state of bioaerosol research, highlights recent advances, and outlines future perspectives in terms of bioaerosol identification, characterization, transport, and transformation processes, as well as their interactions with climate, health, and ecosystems, focusing on the role bioaerosols play in the Earth system.

1. Introduction

Primary biological aerosols (PBA), in short bioaerosols, are a subset of atmospheric particles, which are directly released from the biosphere into the atmosphere. They comprise living and dead organisms (e.g., algae, archaea, bacteria), dispersal units (e.g., fungal spores and plant pollen), and various fragments or excretions (e.g., plant debris and brochosomes; Ariya and Amyot, 2004, Brown et al., 1964, Castillo et al., 2012, Cox and Wathes, 1995, Després et al., 2012, Graham, 2003, Madelin, 1994, Matthias-Maser et al., 1995, Rogerson and Detwiler, 1999, Tesson et al., 2016, Womack et al., 2010). As illustrated in Fig. 1, PBA particle diameters range from nanometers up to about a tenth of a millimeter. The upper limit of the aerosol particle size range is determined by rapid sedimentation, i.e., larger particles are too heavy to remain airborne for extended periods of time (Hinds, 1999, Pöschl, 2005).

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Fig. 1. Characteristic size ranges of atmospheric particles and bioaerosols with exemplary illustrations: (A) protein, (B) virus, (C) bacteria, (D) fungal spore, and (E) pollen grain (adapted from Pöschl and Shiraiwa, 2015). Image A is a model simulation of BetV1 (Kofler et al., 2012, Xu and Zhang, 2009) created with PDB protein workshop 3.9 (Moreland et al., 2005).

Bioaerosols play a key role in the dispersal of reproductive units from plants and microbes (pollen, spores, etc.), for which the atmosphere enables transport over geographic barriers and long distances (e.g., Brown and Hovmøller, 2002, Burrows et al., 2009a, Burrows et al., 2009b, Després et al., 2012, Womack et al., 2010). Bioaerosols are thus highly relevant for the spread of organisms, allowing genetic exchange between habitats and geographic shifts of biomes. They are central elements in the development, evolution, and dynamics of ecosystems.

An overview of bioaerosol cycling and effects in the Earth system is given in Fig. 2. Some organisms actively emit PBA particles, such as wet-discharged fungal spores, which are emitted with the help of osmotic pressure or surface tension effects, while the passive emission of other PBA particles, like thallus fragments and dry-discharged fungal spores, is mostly wind-driven (Elbert et al., 2007). In the atmosphere, PBA undergo internal and external mixing with other aerosols, including biogenic secondary organic aerosol (SOA) formed upon oxidation and gas-to-particle conversion of biogenic volatile organic compounds, which can influence bioaerosol properties through SOA coatings on PBA particles (Hallquist et al., 2009, Huffman et al., 2012, Pöhlker et al., 2012b, Pöschl et al., 2010).

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Fig. 2. Bioaerosol cycling in the Earth system. After emission from the biosphere, bioaerosol particles interact with other aerosol particles and trace gases in the atmosphere and can be involved in the formation of clouds and precipitation. After dry or wet deposition to the Earth’s surface, viable bioparticles can contribute to biological reproduction and further emission. This feedback can be particularly efficient when coupled to the water cycle (bioprecipitation).

Adapted from Pöschl and Shiraiwa (2015) and Pöschl (2005).

It is still an open question whether there are sufficient numbers of CCN- and IN-active bioaerosols at cloud altitudes to affect cloud formation and evolution. However, in pristine air over vegetated regions or under remote conditions, bioaerosols might represent a significant fraction of CCN and IN and are likely to be an essential regulating factor in the formation of clouds and precipitation (Andreae and Rosenfeld, 2008, Healy et al., 2014, Huffman et al., 2013, Pöhlker et al., 2012b, Pöschl et al., 2010). Moreover, Creamean et al. (2013) found by direct cloud and precipitation measurements that long-range transported dust mixed with biological residues plays an important role in cloud ice formation and precipitation processes over the western United States. Wright et al. (2014) proposed that increasing relative humidity, due to a cold-frontal passage, could trigger the release of biological IN, which in turn may seed the frontal cloud band. Increasing concentrations of bioaerosols and IN during and after rain events have been found in a forest ecosystem (Fig. 12; Huffman et al., 2013, Prenni et al., 2013, Tobo et al., 2013).

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Fig. 12. Aerosol properties during dry periods and rain events: (A, B) fluorescence microscope images of aerosol impactor samples, (C, D) size distributions of IN and of fluorescent bioparticles, and (E, F) number concentrations of IN plotted against fluorescent bioparticles (Huffman et al., 2013).

Fig. 12A and B shows microscopic images of aerosol impactor samples highlighting the contrast between irregularly shaped dust in a sample collected during dry weather and cellular structures in a sample collected during a rain event. During dry weather conditions dominated by dust, the concentrations of IN at − 15 °C were between 0.01 and 0.02 L^− 1, and no correlation with FBAP concentration was found (Fig. 12C and E). In contrast, during rain events, the size distribution of IN exhibits a distinct peak in the range of 2–6 μm that coincides with the peak of the size distribution of FBAP (Fig. 12D). Furthermore, the measured IN concentrations followed a close linear correlation with FBAP concentration (Fig. 12F). The strong contrast between dry and rainy periods suggests that the release of PBA during and after rain may play an important role in the spread and reproduction of microorganisms in certain environments, and it may also contribute to the atmospheric transmission of pathogenic and allergenic agents (Fig. 13A; Huffman et al., 2013).

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Fig. 13. Bioprecipitation cycle. Terrestrial ecosystems are the major source of ice nucleation active microorganisms; precipitation and humidity can enhance bioparticle emissions (rain splash, active wet discharge, etc.); bioparticles serving as ice nuclei or giant cloud condensation nuclei (IN/GCCN) can influence the evolution of clouds and precipitation, which provide water for growth of vegetation and for multiplication of microorganisms (A, B). Deposition of pathogenic and allergenic species can trigger human, animal and plant diseases (A; Huffman et al., 2013). Ice nucleation activity of microorganisms is positively selected in various ecosystems, on frost damaged plants and with precipitation itself.

Fig. 19 shows an overview of important and promising areas of future research, which can be coarsely divided into the three main fields: (1) bioparticle identification and characterization; (2) atmospheric transport and transformation; and (3) ecosystem interactions of bioaerosols. Studies within these fields could help to close or narrow the large gaps of knowledge outlined in this review and to constrain uncertain parameters and assumptions, which will allow to improve modeling of the effects of bioaerosols on climate, health, and ecosystems on local, regional, and global scales.

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  For comprehensive taxonomic and chemical identification, characterization, and quantification of bioaerosol particles, their viability and metabolic state, the wide range of advanced and innovative online and offline measurement methods outlined in Sect. 2 should be applied and further developed (NGS sequencing, fluorescence detection, etc.). An important aspect is the coupling of detailed biological analyses and information with the real-time data of modern physical and chemical techniques, including genomic, proteomic, and metabolomic approaches. The development and application of standardized sampling and analysis techniques appears necessary to achieve consistency between different measurements and datasets.

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  To understand the spatial and temporal dynamics of atmospheric bioaerosols, the pathways of emission, transport, and transformation in the atmosphere need to be analyzed from molecular to global scales. Major challenges include the quantitative characterization of exchange between surface, planetary boundary layer, and free troposphere. For this purpose, ground based measurements have to be combined with tall tower and aircraft measurements as well with satellite remote sensing to obtain information on the vertical and horizontal distribution of bioparticles. Particularly interesting are the distribution patterns of IN-active microorganisms and detached nanometer-sized IN-active particle fragments and macromolecules (also called “nano-INP” or “INM”), and their interactions with clouds and precipitation. These have to be elucidated on microscopic as well as regional and global scales to validate or discard the bioprecipitation feedback hypothesis and its relevance for the Earth system (Sect. 3.3). Other important aspects are the effects of physical, chemical, and biological transformation, aging, and stress upon exposure to atmospheric oxidants, radiation, and changes of temperature, pressure, and humidity (osmotic shock) on the emission, vitality, and viability of airborne bioparticles. These effects need to be quantified in chamber and field studies under relevant conditions to fully understand the impact of atmospheric transport on the adaptation and resilience of aerially disseminated organisms (wind-pollinated plants, sporulating microbes) and their influence on the functioning of ecosystems.

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  Representative measurements and climatologies of bioaerosols in and above ecosystems along the climatic gradients from tropical to polar and continental to marine regions are required to unravel the interdependence of biodiversity and biogeography in the air and at the Earth surface, as well as the impact of environmental conditions, climate, and land use change on bioaerosol emission and deposition, related biogeochemical cycles, and public health. Key aspects are the roles of cryptogamic covers on ground and plant surfaces, nitrogen cycling microbes, and bioprecipitation feedbacks in the co-evolution of life and climate, as well as the spread and effects of pathogens and allergens interacting with air pollutants. To address these issues, the results of comprehensive observations and bioaerosol monitoring in today’s atmosphere (e.g., by NGS sequencing, fluorescence detection, and chemical analysis) should be compared and combined with climate archive analyses (e.g., pollen, spores, biomarkers, and DNA in lake and ocean sediments) and implemented in ecosystem and Earth system models. Ecosystem and Earth system model descriptions and parameterizations of all bioaerosol properties and processes outlined above are relevant for our understanding of the origins and spread of life on Earth and for the modeling of ecosystem interactions in Earth’s history and future climate.

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Fig. 19. Key aspects and areas of research required to determine and quantify the interactions and effects of biogenic aerosol particles in the Earth system, including primary biological aerosols (PBA) directly emitted to the atmosphere and secondary organic aerosols (SOA) formed upon oxidation and gas-to-particle conversion of volatile organic compounds (VOC).

Bioaerosols and their importance for low-level Arctic clouds

Gabriel Pereira FreitasAcademic dissertation for the Degree of Doctor of Philosophy in Environmental Sciences at Stockholm University to be publicly defended on Friday 15 December 2023 at 13.00 in De Geersalen, Geovetenskapens hus, Svante Arrhenius väg 14.

Abstract

Bioaerosols are microorganisms or functional parts of them or other biological matter suspended in air. Examples are bacteria, viruses, pollen, spores, or smaller plant debris. In the atmosphere, bioaerosols can play various functional roles, such as facilitating the spread of genetic material. Moreover, they can play an important role in climate by serving as ice nucleating particles and thus participating in cloud formation. Bioaerosols might play a significant role in a changing Arctic, where aerosol concentrations can be very low, and where natural as well as anthropogenic aerosol sources are subject to drastic changes due to climate change. In the Arctic, aerosols and clouds are prominent actors in climate by mediating short- and long-wave radiation interactions, which are further complicated by the presence of high-albedo surfaces such as sea ice. Thus, constraining the sources of aerosols and their interaction with clouds is key to understanding the Arctic climate and the changes it has been and will undergo.

In this work, we used a single-particle instrument to differentiate bioaerosols from other particles on the basis of their fluorescence and light-scattering signal. In the Baltic Sea, we found that bioaerosols are at least 1 in every 104 coarse particles emitted by sea spray. Their temporal emission pattern was not directly correlated with biological tracers, such as chlorophyll; instead, their emission was modulated by the transition between different water masses.

The same technique was then applied to a one-year measurement campaign at an Arctic mountain top observatory as part of a greater aerosol-cloud interaction campaign. The recorded seasonal cycle of bioaerosol concentrations peaked in summer and was most likely related to regional terrestrial sources, as its appearance coincided with a decrease in snow cover and an increase in vegetation activity. Moreover, bioaerosols were found to drive the concentration of high-temperature ice nucleating particles, even in winter. In the third study, the importance of bioaerosols serving as cloud seeds was investigated by directly measuring the concentration of bioaerosols within cloud residuals.

The presented findings help to elucidate the contribution of bioaerosols to coarse-mode particles for marine and Arctic environments, while also providing a direct link between bioaerosols and clouds. Furthermore, we also provide the first direct observations of bioaerosols involved in cloud formation in the Arctic, along with their possible contribution to the prevalence of mixed-phase clouds in the beginning and end of summer. Thus, these results contribute to a better understanding of atmospheric (bio-)aerosol-cloud-interactions processes in the vulnerable Arctic environment but are also valuable for further developments of Earth system models that include ice nucleating and/or bioaerosol particles.

Keywords: Bioaerosols, Aerosols, Clouds, Arctic, Cloud Condensation Nuclei, Ice Nucleating Particles, Sea Spray Aerosol.

Stockholm 2023 http://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-223503