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. 2023 Jul 10;57(29):10512–10520. doi: 10.1021/acs.est.3c01368

Will “Air Eutrophication” Increase the Risk of Ecological Threat to Public Health?

Yan-Feng Sun †, Yuming Guo ‡,§, Chi Xu ∥, Ying Liu †, Xu Zhao †, Qian Liu ⊥, Erik Jeppesen †,¶,□,■,○, Haijun Wang †,*, Ping Xie †,●,*
PMCID: PMC10373653  PMID: 37428654

Abstract

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Aquatic eutrophication, often with anthropogenic causes, facilitates blooms of cyanobacteria including cyanotoxin producing species, which profoundly impact aquatic ecosystems and human health. An emerging concern is that aquatic eutrophication may interact with other environmental changes and thereby lead to unexpected cascading effects on terrestrial systems. Here, we synthesize recent evidence showing the possibility that accelerating eutrophication will spill over from aquatic ecosystems to the atmosphere via “air eutrophication”, a novel concept that refers to a process promoting the growth of airborne algae, some of them with the capacity to produce toxic compounds for humans and other organisms. Being catalyzed by various anthropogenic forcings—including aquatic eutrophication, climate warming, air contamination, and artificial light at night—accelerated air eutrophication may be expected in the future, posing a potentially increasing risk of threat to public health and the environment. So far knowledge of this topic is sparse, and we therefore consider air eutrophication a potentially important research field and propose an agenda of cross-discipline research. As a contribution, we have calculated a tolerable daily intake of 17 ng m–3 day–1 for the nasal intake of microcystins by humans.

Keywords: air eutrophication, airborne algae, microcystins, public health

Short abstract

Minimal research has been done on airborne algal toxins. This study reports that “air eutrophication” may be accelerated under the catalyst of anthropogenic forcings, posing a threat to public health and the environment.

Aquatic Eutrophication, Cyanotoxins, and Their Health Impacts

The great acceleration of the Anthropocene leaves severe imprints on our biosphere.1,2 Aquatic eutrophication induced by excessive inputs of nutrients (e.g., nitrogen and phosphorus) is among the most conspicuous of the anthropogenic forcings.3,4 Thus, eutrophication has profoundly impacted aquatic ecosystems and societies and led to, i.a., water quality deterioration, biodiversity loss, and human health problems caused by toxins produced by harmful algal blooms. This has resulted in declines of various ecosystem services,5,6 which compromises the UN’s Sustainable Development Goals. Cyanobacteria can produce a variety of toxins called cyanotoxins, such as microcystin (MC), which are detrimental and even lethal to invertebrates, fish, birds, and mammals7,8 (see more in Chart 1). Microcystin-leucine-arginine (MC-LR) is one of the most toxic and common microcystin variants.9 For humans, oral and dermal contact with water containing high concentrations of cyanobacterial toxins can lead to hepatic dysfunction and other digestive maladies.10 In 1996, contamination of water supplies with cyanotoxins resulted in the death of more than 60 people in the hemodialysis unit in Caruaru, North-East Brazil.11 To protect public health, the World Health Organization has proposed a guideline value of MC-LR below 1 μg L–1 in drinking water.12

Chart 1. Types of Cyanotoxins and Toxicity of Microcystins.

Chart 1

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Another additional concern is that eutrophication may interact with other anthropogenic forcings and thereby have led to unexpected cascading environmental changes such as a spillover effect of aquatic eutrophication to terrestrial systems catalyzed by climate change. Promoted by increased frequency and intensity of hot-dry climate extremes, massive growth of cyanobacteria in waters elevates cyanotoxins to extreme levels that may be lethal to terrestrial megafauna. Examples of this are the mass death of African elephants in Botswana in 2020, which was attributed to an amplified effect of eutrophication and harmful cyanobacterial blooms,13 and the death of bald eagles (Haliaeetus leucocephalus) in Lake DeGray, Arkansas, after feeding on fish and waterfowl containing cyanotoxins cascading from cyanobacteria through the food chain.14

Airborne Algae, Algal Toxins, and the Risk of Impacts on Public Health

Algae can be emitted from aquatic ecosystems into the atmosphere by wind-driven or ecosystem disturbances linked to animal movement and human activity15−17 (Figure 1). Once emitted, the algae will be further dragged into the atmosphere by airborne turbulent kinetic energy,18 even into the troposphere.19 Recent studies have shown that 10% of microbes, including algae (0.5–5 μm in size) emitted from the sea, remain in the air 4 days after emission and that they can travel up to 11 000 km.20 Airborne algae have also been detected in indoor environments.21 Inhalation of these small-sized airborne algae is potentially harmful to animals and humans as they are deposited in the respiratory tract.22 A high occurrence frequency of algae was observed in the upper respiratory tract in 92% of 77 study individuals who received a nasal swab and in the central airways in 79% of 29 individuals inspected with bronchoscopy, suggesting that airborne algae can be lodged in the nostrils and lungs after inhalation.23

Figure 1.

Figure 1

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Development of “air eutrophication” and the potential impacts on human health and the maximum concentrations of microcystins measured in aerosols surrounding lakes. Aquatic eutrophication along with excessive nutrient loading promotes massive growth of algae, some of which are toxin-producing cyanobacteria. Aquatic algae can be emitted to the atmosphere where they form airborne assemblages. Air eutrophication develops along with the aquatic eutrophication and thereby provides algae sources, air contamination provides nutrients for airborne algae, and climate warming and artificial light at night stimulate the growth. Airborne algae and cyanotoxins can enter the body through human respiration, posing a potential threat to human health. Maximum concentrations of microcystins measured in aerosols surrounding lakes (see Chart 2 for the derivation of TDI—tolerable daily intake; see refs (25 and 73−77) for the source of measured aerosol microcystins).

Phytoplankton-generated aquatic toxins can be transferred to the air through aerosolization.17 In addition, algal toxins produced by certain airborne algae constitute an important threat to human health.24 In situ measurements in some lakes suggested a range of cyanotoxins between 0.00023 and 50 ng m–3 in aerosols (Figure 1, Table 1). When spraying lake water containing 230 μg L–1 MC into the air in the lab, MC in aerosol samples reached a level as high as 50 ng m–3.25 When female larval fruit flies (Drosophila melanogaster) were exposed to aerosolized cyanobacteria blooms, reduced lifespan and significant signs of cerebral degeneration were observed.26 In mice where MC-LR was administered by inhalation or intratracheally, necrosis of the respiratory epithelium, bleeding in the liver, and damage to kidneys and intestines were observed.27,28 For humans, inhalation of airborne algae and algal toxins may cause skin irritation, allergies, rhinitis, and respiratory problems29 (Figure 1).

Table 1. Collected Studies on Cyanotoxin Concentrations in Aerosolsa.

cyanotoxin aquatic microcystin (μg/L) airborne microcystin (ng/m3) quantification method aerosol collection method source of water studied study location reference
microcystin 50 0.2 ELISA personal sampler laboratory laboratory (74)
microcystin 2.125 0.05 ELISA high-volume sampler field Lake Bear, Michigan (74, 75)
2.625 0.023
3 0.057
microcystin 82.275 0.0052 ELISA high-volume sampler field Bloom Lake 1, California (76)
82.275 0.4 personal sampler Bloom Lake 2, California
142.75 0.1
67.525 0.2
microcystin 230 50 LC-MS/MS lake spray aerosol generator field (Lake Mona, AU) laboratory (25)
microcystin 155.987 0.0003 ELISA high-volume sampler field Lake Rotorua, South Island, NZ (77)
1548.529 0.0018
447.839 0.0009
nodularin 4.718 0.0073 Lake Forsyth, South Island, NZ
0.952 0.00023
anatoxin-a 21 0.16 LC-MS/MS air sampling device field Capaum Pond, Massachusetts (78)
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a

Note: Data are average values.

Despite their aquatic origin, most cyanotoxins tended to be more hazardous to terrestrial mammals (the median lethal dose of MC-LR by the intraperitoneal route was i.p. LD50 = 50 μg kg–1 for tested mice) than to aquatic biota (i.p. LD50 = 270–790 μg kg–1 for the tested fish Hypophthalmichthys molitrix and Oreochromnis niloticus).30 Furthermore, toxin inhalation might be more dangerous than oral intake as suggested by the observed median lethal dose of 250 μg kg–1 MC-LR through intratracheal administration to mice compared to 3000 μg kg–1 MC-LR through oral administration.25,31 Inhalation of MC-LR in mice was found to induce necrosis of the respiratory epithelium, which further promoted the absorption of the toxin into the bloodstream.27 Inhalation directly impacts the respiratory system, and inhaled toxins can directly enter the organs. In addition, studies on the immunological effects of vaccines by different routes of administration have revealed that inhaled aerosol vaccines provide better protection and stimulate stronger immune responses than nasal spray vaccines.32 The inhaled aerosol passes through the nasal passage and delivers the vaccine droplets deep into the airways, inducing a broad protective immune response.33 This also reinforces the view that nasal inhalation of aerosolized algae and algal toxins may have more potent toxic effects. To test this, we calculated a tolerable daily intake (TDI) of 17 ng m–3 day–1 for the nasal intake of MC-LR in humans, based on the TDI in mice18 and the average human body weight (60 kg body weight, 7 m3 of air inhaled per day)34 (see Chart 2 for the derivation of TDI).

Chart 2. TDI of MC-LR for Humans.

Chart 2

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Multiple Drivers Potentially Accelerating Air Eutrophication

There is growing evidence that algal blooms in eutrophic aquatic ecosystems have increased in diversity, frequency, size, and geographical extent in recent decades,35 implying an enriched source of airborne algae.36,37 Climate warming, with the additional light hours and richer light intensities provided by artificial light at night (ALAN), may directly favor the formation, transportation, and development of airborne algae and increase the potential of toxin production and hence the risk of human exposure to toxins. In the future, humans and wildlife are expected to face an increasing risk of exposure to airborne algae and the cyanotoxins that they produce in cyanobacteria-impacted aquatic ecosystems.

It is widely recognized that eutrophication is accelerating in response to global warming, particularly in recent years.38,39 Widespread, prolonged, and unprecedented extreme heat has occurred in 2022 in the Northern Hemisphere, exceeding the expectations of many climate scientists.40 The preliminary results of a study of airborne algae conducted in the southern coastal zone of the Baltic Sea from January to December 2022 suggest that the total amount of airborne cyanobacteria was positively correlated with the concentration of MC-LR, and the increase of airborne cyanobacteria and airborne algae was mainly related to the rise in temperatures.41 The proportion of toxic species or strains and the release of toxins tend to increase in a hotter climate,42,43 potentially enhancing the risk of airborne algal toxin production. Climate warming may also favor the growth and competition of small-sized freshwater and marine algae species,44,45 which are more likely to be emitted into the atmosphere and carried to distant locations away from their sources than large-sized species.46

Light availability is another key factor controlling the growth of algae in aquatic ecosystems.47 Urbanization has led to rapid expansion of ALAN in space at a rate of 2–6% per year.48−50 With the advent of a wide range of lighting devices, both cool and warm white ALAN has become increasingly abundant.51,52 For freshwater cyanobacteria, warmer white ALAN means a higher photosystem II:photosystem I ratio and hence stronger photosynthesis activities.53 A positive correlation was observed between photosynthetically active radiation and toxin production in Microcystis aeruginosa.54 The proportion of cyanobacteria was found to increase by 17%, while the proportion of diatoms and chrysophytes decreased in spring when exposed to ALAN.55 A study conducted in the southern Baltic Sea region from 2018 to 2020 showed a positive effect of increased light intensity on the growth of the cyanobacterium Nostoc sp. and the diatoms Nitzschia sp., Amphora sp., and Halamphora sp.56 Therefore, the expansion of ALAN may have a positive effect on the development of “air eutrophication” through enhancing the growth of airborne algae: stimulating the growth of some algae and the production of algal toxins in the aquatic ecosystem, hence providing a richer source of algal and toxin emissions to the atmosphere.

Atmospheric deposition of pollutants has received attention as an important nutrient source for phytoplankton in aquatic ecosystems.57 The contribution of airborne particles is high and increasing in various nutrients such as nitrogen, phosphorus, and carbonaceous compounds.58−60 A global increase of 12.8 ± 1.3% of atmospheric ammonia (NH3) was recorded between 2008 and 2018.61 Significant increases in nitrogen dioxide (NO2) and reactive volatile organic compounds have also been widely reported, particularly in tropical cities.62 It has been shown that nitrogen-enriched acid rain and anthropogenic atmospheric nitrogen deposition can enhance marine primary production.63,64 For example, it was found that atmospheric dry deposition of nutrients along the coastal Bay of Bengal resulted in an increase in primary production from 3% to 19%.65 Aerosol deposits from wildfires, metals carried by volcanic lava, and deposition of nitrogen and phosphorus from burning fossil fuels have also been reported to stimulate the growth of aquatic phytoplankton.66,67 But what about the stimulation of the growth of airborne algae? A strong positive correlation was found between aerosol bacterial gene abundance and air pollutant concentrations and the air quality index in a study on the atmosphere of Hefei City, China.68 Whether a similar direct stimulating effect on the development of airborne algae and toxins occurs with increasing nutrient pollution in the air is an open question but important to elucidate given the potential health problems associated with some algae and their toxins in regions with high production of such algae in the water.

In contrast to the widely reported fundamental role of nutrients in the growth of aquatic algae, few studies are available on airborne algae, unfortunately.

Urgent Need for Research into Air Eutrophication and Development of Solutions

Currently, little research has been carried out on airborne algae, their prevalence, and impacts. However, we cannot wait for consensus based on ample evidence when it comes to potentially major threats to public health. Atmospheric bacteria and fungi are an important component of bioaerosols, and their community composition is influenced by a complex set of environmental factors.69 At the same time, they are more abundant than airborne algae and can pose a serious threat to human health and the environment as pathogens and allergens.70,71 As such, atmospheric bacteria and fungi will also play a non-negligible role in promoting air eutrophication. Therefore, we consider “air eutrophication” as a potentially important research field requiring a cross-discipline research effort, including medical, physical, hydrological, geological, and ecological expertise (Chart 3). This research agenda is timely for applying the precautionary principle as a critical risk management strategy for ensuring the safety of public health and the environment worldwide, particularly in the areas with extremely high risk of cyanotoxin exposure and climate changes.72

Chart 3. Research Agenda.

Chart 3

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Acknowledgments

We thank Prof. Hans W. Paerl for his editorial contribution and valuable comments and Anne Mette Poulsen for English editions. This research was supported by the Yunnan Provincial Department of Science and Technology (202001BB050078; 202103AC100001). H.W. was supported by the Youth Innovation Association of the Chinese Academy of Sciences as an excellent member (Y201859). E.J. was supported by the TÜBITAK program BIDEB 2232 (project 118C250). Y.G. was supported by the Career Development Fellowship (number APP1163693) and Leader Fellowship (number APP2008813) of the Australian National Health and Medical Research Council. C.X. was supported by the National Natural Science Foundation of China (No. 32061143014) and the Fundamental Research Funds for the Central Universities of China.

Biographies

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Prof. Dr. Haijun Wang has been working on aquatic eutrophication and cyanobacteria bloom for 22 years. Before moving to Yunnan University with a Grant of High-level Talented Scientist, he had been working for 20 years at the Institute of Hydrobiology, Chinese Academy of Sciences. He is now the deputy director of Institute for Ecological Research and Pollution Control of Plateau Lakes, School of Ecology and Environmental Sciences, Yunnan University. He was selected as an excellent member of the Youth Innovation Promotion Association of Chinese Academy of Sciences in 2018.

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Prof. Dr. Ping Xie is a principal scientist at the Institute of Hydrobiology, Chinese Academy of Sciences, and is the director of Water Subcenter of Chinese Ecosystem Research Network (CERN) and vice director for the State Key Laboratory of Freshwater Ecology and Biotechnology, China, and the dean of Institute for Ecological Research and Pollution Control of Plateau Lakes, School of Ecology and Environmental Sciences, Yunnan University. He has very strong background in aquatic eutrophication, cyanobacteria blooms, and ecological impacts of cyanobacteria and cyanotoxins. Prof. Xie received his Ph.D. from University of Tsukuba, Japan, in 1989. He won an international award, Biwako Prize for Ecology, in 1999. He has published more than 250 SCI-indexed papers as the first or corresponding author. His articles have been cited over 10 000 times with an H index of 50. From 2014 to 2021, he has been on the list of highly cited Chinese scholars in Environmental Science or Biology released by Elsevier.

Author Contributions

Y.F.S., Y.G., and H.W. conceptualized and designed the study. Y.F.S. and H.W. visualized the tables and figures and wrote the original draft manuscript. Y.G., C.X., Y.L., X.Z., Q.L., E.J., H.W., and P.X. reviewed and edited the manuscript. All authors revised the manuscript, approved the final manuscript, and agreed to take responsibility for all aspects of the work.

The authors declare no competing financial interest.

Special Issue

Published as part of the Environmental Science & Technologyvirtual special issue “The Exposome and Human Health”.

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