Environment International 145 (2020) 106156 Contents lists available at ScienceDirect Environment International journal homepage: www.elsevier.com/locate/envint Review article Airborne bacterial communities of outdoor environments and their associated influencing factors Tay Ruiz-Gil a,b, Jacquelinne J. Acuna~ b,c,e, So Fujiyoshi b,c,d,e, Daisuke Tanaka f, Jun Noda e,g, Fumito Maruyama b,c,d,e, Milko A. Jorquera b,c,e,* a Doctorado en Ciencias de Recursos Naturales, Facultad de Ingeniería y Ciencias, Universidad de La Frontera, Temuco, Chile b Laboratorio de Ecología Microbiana Aplicada (EMALAB), Departamento de Ciencias Químicas y Recursos Naturales, Universidad de La Frontera, Temuco, Chile c Network for Extreme Environment Research (NEXER), Scientific and Technological Bioresource Nucleus (BIOREN), Universidad de La Frontera, Temuco, Chile d Microbial Genomics and Ecology, Office of Industry-Academia-Government and Community Collaboration, Hiroshima University, Hiroshima, Japan e Center for Holobiome and Built Environment (CHOBE), Hiroshima University, Japan f Graduate School of Science and Engineering, University of Toyama, Toyama, Japan g Graduate School of Veterinary Science, Rakuno Gakuen University, Hokkaido, Japan ARTICLE INFO ABSTRACT Handling Editor: Xavier Querol Microbial entities (such bacteria, fungi, archaea and viruses) within outdoor aerosols have been scarcely studied compared with indoor aerosols and nonbiological components, and only during the last few decades have their Keywords: studies increased. Bacteria represent an important part of the microbial abundance and diversity in a wide va­ Airborne bacteria riety of rural and urban outdoor bioaerosols. Currently, airborne bacterial communities are mainly sampled in Atmosphere two aerosol size fractions (2.5 and 10 µm) and characterized by culture-dependent (plate-counting) and culture- Bacterial communities independent (DNA sequencing) approaches. Studies have revealed a large diversity of bacteria in bioaerosols, Bioaerosols Outdoor environments highlighting Proteobacteria, Firmicutes, Actinobacteria and Bacteroidetes as ubiquitous phyla. Seasonal varia­ tions in and dispersion of bacterial communities have also been observed between geographical locations as has their correlation with specific atmospheric factors. Several investigations have also suggested the relevance of airborne bacteria in the public health and agriculture sectors as well as remediation and atmospheric processes. However, although factors influencing airborne bacterial communities and standardized procedures for their assessment have recently been proposed, the use of bacterial taxa as microbial indicators of specific bioaerosol sources and seasonality have not been broadly explored. Thus, in this review, we summarize and discuss recent advances in the study of airborne bacterial communities in outdoor environments and the possible factors influencing their abundance, diversity, and seasonal variation. Furthermore, airborne bacterial activity and bioprospecting in different fields( e.g., the textile industry, the food industry, medicine, and bioremediation) are discussed. We expect that this review will reveal the relevance and influencing factors of airborne bacteria in outdoor environments as well as stimulate new investigations on the atmospheric microbiome, particularly in areas where air quality is a public concern. 1. Introduction homologous words when using limited terms as keywords, as illustra­ tion, we carried out a search on the Web of Science database (Fig. 1) Aerosols are defined as suspended particles in the air, with ‘bio­ based on the keywords “aerosol” and “bioaerosol”, and we determined aerosols’ being those with a biological origin. Nonbiological aerosols (e. the number of studies that used the terms “outdoor” and “indoor” over g., dust, ash, heavy metals, sulfur oxides and organic compounds) have the years. While aerosols have been studied during the last one hundred been extensively studied due to their negative effects on public health years, reaching approximately 7,000 published articles to date, bio­ and natural ecosystems (Camatini et al., 2017; Grennfelt et al., 2019; aerosols have 30 years of research and approximately 240 articles Tang et al., 2018; Tomasi et al., 2017). Despite the inherent limitations published to date. At the global level, bioaerosols represent a quarter of that online search engines possess due to the high number of the aerosol mass (Despres´ et al., 2012), and several investigations have * Corresponding author at: Departamento de Ciencias Químicas y Recursos Naturales, Universidad de La Frontera, Ave. Francisco Salazar 01145, Temuco, Chile. E-mail address: [email protected] (M.A. Jorquera). https://doi.org/10.1016/j.envint.2020.106156 Received 26 May 2020; Received in revised form 20 September 2020; Accepted 21 September 2020 Available online 8 October 2020 0160-4120/© 2020 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). T. Ruiz-Gil et al. Environment International 145 (2020) 106156 revealed their prominent roles in climate, ecosystem health and atmo­ 2012). In addition, the ice nucleation activity of airborne bacteria (most spheric processes (Morris et al., 2014; Frohlich-Nowoisky¨ et al., 2016). of which are reported as phytopathogens) may induce ice and cloud However, most bioaerosol studies have concentrated on indoor envi­ formation, which promotes precipitation, altering the climate and mi­ ronments (Gao et al., 2015; Fujiyoshi et al., 2017; Kim et al., 2018). As crobial biogeographical dispersion (Bigg et al., 2015; Christner et al., shown in Fig. 1, despite an increase in aerosol and bioaerosol studies 2008). Studies have also revealed that airborne bacterial composition during recent years, research on bioaerosols in outdoor environments and dispersion in the atmosphere can be influenced by specific micro- accounts for the lowest proportion of studies. and macroscale determinants, such as land use, emission sources, con­ Within bioaerosols, we mainly find isolated or associated microbial centration and particle size, air humidity, wind speed, and temperature ˇ entities (bacteria, fungi, protozoa, algae, archaea and viruses), solid (Fujiyoshi et al., 2017; Bowers et al., 2011; Gandolfiet al., 2015; Santl- fragments or excretions of organisms, plant debris, leaf litter and pollen. Temkiv et al., 2018). Anthropogenic activities (e.g., farming and waste treatment plants) and A recent review of airborne bacterial communities has described natural processes (e.g., sea spray, pollination, volcanic eruption, wild­ factors influencing bacterial concentrations and communities in built firesand desert dust) have been described as principal emission sources environments, proposing the establishment of a standard procedure for of bioaerosols into the atmosphere (Tomasi et al., 2017; Despr´es et al., the study of indoor airborne bacteria using four factors (temperature, 2012). Similarly, concentrations and dispersion ranges are determined relative humidity, air exchange rate, and occupant density) (Fujiyoshi by physicochemical (e.g., particulate matter size and concentration) and et al., 2017). However, atmospheric factors regulating airborne bacterial meteorological (e.g., wind speed, relative humidity, temperature and communities in outdoor environments at the local and global levels as solar radiation) conditions (Bertolini et al., 2013; Zhen et al., 2017). well as bacterial taxa that can serve as microbial indicators of specific Since biological components can exist from <0.1 µm for viruses, 1 to 10 bioaerosol sources and seasonality need to be demonstrated in both µm for bacteria, vegetative cells, and spores, and up to 100 µm for plant urban and rural environments. In this review, we provide a current pollens, they distribute in a wide range of particle sizes. Moreover, those overview of the advances in the study of airborne bacterial communities biological components may agglomerate by themselves and/or attach to in outdoor environments and the possible factors influencing their abiotic particles in the air. The atmosphere is categorized as an extreme abundance, diversity and seasonal variation in diverse outdoor envi­ environment where nonbiological aerosol particles can serve as refuges ronments. In addition, the activity and potential biotechnological ap­ and energy sources for airborne microorganisms; the abundance and plications of airborne bacteria are discussed. diversity of airborne microorganisms are highly influenced by the type of suspended nonbiological particles and their sizes (Bowers et al., 2013; 2. Study of airborne bacterial communities Cao et al., 2014; Fujiyoshi et al., 2017; Tanaka et al., 2020). High airborne microbial concentrations, from 103 to 107 cells m 3 of air Traditionally, bacterial communities in bioaerosols have been stud­ (Gandolfi et al., 2013; Maki et al., 2017), can be found from mountain ied using culture-based methods, but it is widely known that culture peaks to desert dust clouds. Some metagenomics studies have also re­ media capture only a small fraction of the total environmental bacteria, ported notable relative abundances of bacterial reads in aerosols sam­ and the same trend has been observed for bioaerosols (Gandolfi et al., ples (Bowers et al., 2013; Cao et al., 2014). 2013; Duquenne, 2018). DNA-based methods are currently used to un­ In general terms, human