Spore liberation: How and why fungal spores move through the air

When do fungi release spores? How far might these spores travel? Will these spores survive for a prolonged period? These are questions of importance to microbiologists in many sectors (including pharmaceuticals and healthcare), especially for understanding the contamination potential and seeking to improve building design and other contamination control practices.

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Answering this is not easy and research on fungal dispersal often falters on the subject of dispersal dynamics. Researchers have not been able to develop a unifying paradigm of fungal dispersal and the accuracy associated with such attempts decreases relative to the lengthening of the distance. That said, there are variables that we can consider that affect fungal spore dispersal and survival.

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The focus of this article is on the ascomycota, which includes genera like Penicillium, Aspergillus and Candida (1). These fungi tend to reproduce sexually, forming ascospores (2). Some can also produce asexual spores (conidia) called chlamydospores (resting spores), a life stage that has evolved to survive in unfavorable conditions, such as dry or hot seasons (3).

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This week’s article looks at some of the mechanisms impinging upon fungal spore dispersal.

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What is fungal spore dispersal?

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Fungal spores are microscopic biological particles that allow fungi to be reproduced. In one sense this serves a similar purpose to that of seeds in the plant world. Fungal spores are tiny cells that form on special hyphae. These spores are very tiny and around 1,000 could fit on a pinhead.

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Fungal spore release into air is either driven by an active mechanism when the energy is provided by the fungi, or by a passive mechanism when the energy is provided by external sources (like air currents or a physical force).

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Considering the fungi’s own dispersal mechanism, to reach the air, spores need to be forcibly ejected (some describe this as an ‘explosion’). In ascomycete fungi the source is an actively discharging ascus (a saclike structure) which dispatches spores into the atmosphere. This type of ascus is a form of sophisticated pressure gun capable of repeatedly discharging spores at an extremely high velocity (a common range is 0.8 to 1.2 m s–1) (4, 5). Basidiomycete fungi also actively eject their spores.

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The forcibly ejected spores must penetrate several millimeters of nearly still air surrounding the fungal mass in order to reach dispersive airflows. Not all released spores succeed. The likelihood of escape is higher for spores launched with a larger velocity, following what is described as elastohydrodynamic theory (6).

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Spores move in air currents and in the natural environment, fungal spores are spread by the wind. Another mechanism is via water droplets.

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The fungal spore dispersal phase includes the take-off, transport, and eventual deposition of the inoculum (7). On release, spores experience great fluid drag. This drag can aid transport by slowing sedimentation out of dispersive air flows; however, it also causes spores to decelerate rapidly after launch.

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Spore liberation

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When will fungi release spores? How far are they likely to travel? Fungi do not appear to release spores randomly or uncontrollably. Many species seek to maximize survival during atmospheric transport by controlling the release. To better understand what is happening, we need to develop an aerobiological model (8).

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Shape

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Fungal spores are of different shapes and sizes. The dimensions influence the direction and distance of travel. By studying spore shapes scientists can predict the speed of spore launch and likely drag effects (9).

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Time of day

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Some fungi release spores intermittently, while other species release spores at specific times of day (10).

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The timing of spore release dictates how long spores remain in the atmosphere before returning to the ground. Studies have established that spores released at night are likely to travel for hours while spores released during the day may linger for days. These differences are caused by intense turbulence during the day and weak turbulence at night.

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Those fungi that control their spore release often tend to produce higher concentrations of spore at midday. This is seen from research into spore plumes where concentrations increase from lows around 20,000 total spores/m^3 to highs over 170,000 total spores/m^3 (11).

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Climate

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Spore survival is greater in lower, warmer latitudes. This arises because spores in the open atmosphere are likely to die from prolonged exposure to light and air. Further with temperature, spores released during the hottest part of the day are shown to be more likely to undergo long-distance dispersal than those released at other times (12).

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Differences between genera are seen when it comes to humidity. Airborne spore counts Aspergillus and Penicillium are usually higher in dry than moist air, being minimal at relative humidities (r.h.) above 70%. In contrast, Cladosporium appears to have a greater association with higher humidity.

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Aside from temperature and humidity, wind speed and turbulence is a significant influencing factor. Another meteorological factor is when spore plumes appear to be more concentrated due to the changing weather conditions associated with thunderstorms.

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Airflow is the main factor driving aerosolization of fungal spores indoors.

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Can the path taken be predicted?

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Since individual spores follow unpredictable trajectories due to turbulence, the predicted direction cannot be ascertained. Generally, the majority released will be deposited close to the location of the formation. However, during more turbulent conditions, long-distance dispersal of spores is more likely to occur.

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Disturbances

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The aerosolization of fungal spores can also occur when fungal materials are subjected to airflow, vibration, and scratching. The degree of release depends on how well the spores have adhered to the colony via the biological binding force. This is influenced by the growth time of the colony (the time it takes for the colony to mature under certain culture conditions), environmental parameters, and damage to the hyphae under external disturbances.

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Indoors, the operation of an HVAC system and human activities can produce hydraulic action on fungal spores by disturbing the surrounding airflow. Looking at undisturbed colonies, a meta-study review showed that typical indoor air currents can release up to 200 spores cm?2 from surfaces over a 30-minute duration. The type of surface affects this rate, since air turbulence increases the spore release from a rough surface.

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When a disturbance took place, then a vibration at a frequency of 1 Hz at a power level of 14 W was shown to be sufficient to trigger a significant increase in the spore release rate.

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Survival

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The long-distance dispersal of fungi is not only shaped by the physical constraints on travel, but this is also influenced by the ability of spores to survive harsh environments. Of the different fungal spores conidia survive for much longer times compared to sexually produced spores, which deteriorate faster in time.

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Fungi produce many thousands of spores since most spores will not survive, dying where they land due to a lack of water and food. However, where conditions are optimal, and the spore germinates, then fungal colonies can form.

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Food

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If a spore lands where there is moisture and food, it may be able to germinate and produce its hyphae. As the hyphae branch and grow out in all directions from the spore, they form a circle of growth that is called a colony. Many fungi require two such colonies to grow next to each other and for these organisms to mate in order for the fungus to form new spores and thereby to spread further.

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Water

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Indoors, fungi can grow on almost any building material if there is enough moisture available. By this, most fungi require water activity of at least aw=0.65 for growth. The fungal activity increases as the water activity-value approaches aw=1 (freely available water) (13).

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Hence survivability is a combination of the humidity conditions in the environment, air temperature, availability of oxygen, and the presence of organic and inorganic nutritional sources.

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Sunlight

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Researchers who have measured the effect of solar radiation (including ultraviolet A and B) on the spore germinability show that sunlight markedly reduces spore germinability in most species. Here, species with thin‐walled spores were particularly light sensitive (14). Generally, fungal spores are killed following continuous exposure to UV radiation for periods of 6 hours or more (linking back to dispersal patterns, this means spores released outside are more likely to survive when there is considerable cloud cover) (15).

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Read more of Tim Sandle’s work on ResearchGate.

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References

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1.????? Y. Qi, Y. Li, W. Xie, R. Lu, F. Mu, W. Bai, S. Du Temporal-spatial variations of fungal composition in PM2.5 and source tracking of airborne fungi in mountainous and urban regions, Sci. Total Environ., 708 (2020), Article 135027

2.????? Jones, E.B. Gareth; Suetrong, Satinee; Sakayaroj, Jariya; Bahkali, Ali H.; Abdel-Wahab, Mohamed A.; Boekhout, Teun; Pang, Ka-Lai (2015). Classification of marine Ascomycota, Basidiomycota, Blastocladiomycota and Chytridiomycota. Fungal Diversity. 73 (1): 1–72

3.????? Staib, P; Morschh?user, J (2007) Chlamydospore formation in Candida albicans and Candida dubliniensis--an enigmatic developmental programme. Mycoses. 50 (1): 1–12

4.????? X. Noblin, S. Yang, J. Dumais, Surface tension propulsion of fungal spores. J. Exp. Biol. 212, 2835–2843 (2009).

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6.????? J. Fritz, A. Seminara, M. Roper, A. Pringle, M. P. Brenner, A natural O-ring optimizes the dispersal of fungal spores. J. R. Soc. Interface 10, 20130187 (2013).

7.????? J. Golan, A. Pringle, Long-distance dispersal of fungi. Microbiol. Spectr., (2017)

8.????? D. E. Aylor, The role of intermittent wind in dispersal of fungal pathogens. Annu. Rev. Phytopatol. 28, 73–92 (1990).

9.????? M. Roper, R. Pepper, M. P. Brenner, A. Pringle, Explosively launched spores of ascomycete fungi have drag minimizing shapes. Proc. Natl. Acad. Sci. U.S.A. 105, 20583–20588 (2008).

10.? D. Savage, M. J. Barbetti, M. J. MacLeod, M. U. Salam, M. Renton, Timing of propagule release significantly alters the deposition area of resulting aerial dispersal. Divers. Distrib. 16, 288–299 (2010)

11.? M. Burch, E. Levetin, Effects of meteorological conditions on spore plumes. Internat. J. Biometeorol. 46, 107–117 (2002).

12.? D. Savage, M. J. Barbetti, M. J. MacLeod, M. U. Salam, M. Renton, Seasonal and diurnal patterns of spore release can significantly affect the proportion of spores expected to undergo long-distance dispersal. Microb. Ecol. 63, 578–585 (2012).

13.? F.J.J. Segers, H.A.B. W?sten, J. Dijksterhuis Aspergillus niger mutants affected in conidial pigmentation do not have an increased susceptibility to water stress during growth at low water activity, Lett. Appl. Microbiol., 66 (2018), pp. 238-243

14.? V. Norros, E. Karhu, J. Nordén, A. V. V?h?talo, O. Ovaskainen, Spore sensitivity to sunlight and freezing can restrict dispersal in wood decay fungi. Ecol. Evol. 5, 3312–3326 (2015).

15.? M. Parnell, P. J. A. Burt, K. Wilson, The influence of exposure to ultraviolet radiation in simulated sunlight on ascospores causing Black Sigatoka disease of banana and plantain. Int. J. Biometeorol. 42, 22–27 (1998).