Desert crust microorganisms, their environment, and ...

Journal of Arid Environments xxx (2013) 1e7

Contents lists available at ScienceDirect

Journal of Arid Environments journal homepage: www.elsevier.com/locate/jaridenv

Desert crust microorganisms, their environment, and human health James T. Powell a, Aspassia D. Chatziefthimiou b, Sandra Anne Banack a, *, Paul Alan Cox a, James S. Metcalf a a b

Institute for Ethnomedicine, P. O. Box 3464, Jackson, WY 83001, USA Weill Cornell Medical College in Qatar, P. O. Box 24144, Doha, Qatar

a r t i c l e i n f o

a b s t r a c t

Article history: Received 23 May 2013 Received in revised form 30 October 2013 Accepted 20 November 2013 Available online xxx

This article reviews current knowledge on cyanobacteria, the dominant primary producers, and other microorganisms in arid desert environments. These microorganisms have developed an array of adaptations to hot, arid climates with intense UV radiation, extreme diurnal temperature fluctuations, and high soil salinity. Crust microorganisms positively contribute to their harsh ecosystems, by preventing evapotranspiration, fixing nitrogen, and blocking solar radiation. In doing so, desert crust prevents soil erosion and facilitates the establishment of plant species. However, like aquatic cyanobacteria, desert cyanobacteria have the potential to produce toxins linked to human and animal illness. Furthermore, the impact of terrestrial cyanobacterial toxins on human health in desert regions is poorly understood. A largely ignored, but potentially important human exposure route for cyanotoxins in desert environments is through the inhalation of desert crusts during dust storms and anthropogenic activity. Future work in this field should include the characterization of toxins produced in desert regions as well as the presence of toxins in clinical and environmental materials. Ó 2013 Published by Elsevier Ltd.

Keywords: Arid climates Biological soil crust Cyanobacteria Desert environment Inhalation Review Toxins

1. Introduction to desert environments Arid desert land occupies as much as 33% of the global terrestrial surface, much of which surrounds the equator. The Sahara desert alone occupies the same square acreage as the United States. Arid climates are defined by the significant absence of rainfall. Within this climate zone are three generally accepted subcategories: hyper-arid regions, which receive less than 100 mm annual rainfall, arid regions, which receive 100e300 mm annual rainfall and subarid regions, which can receive up to 800 mm annual rainfall. Of these three subcategories, arid is the most common, occupying 14.6% of the world’s land area (FOA Forest, 1989). While rainfall averages are useful in generalizing the arid climate, there are also vast exceptions in drought/rainfall cycles. The Atacama Desert in Chile suffered a 400-year drought, interrupted in 1971 by a torrential downpour. The Atacama, one of the driest deserts in the world, is considered the physiological dryness limit for life (Davila et al., 2008). What little precipitation does occur in such harsh environments is not always available to the

* Corresponding author. E-mail address: [email protected] (S.A. Banack).

plant and animal life. Long drought seasons create hard crusts on desert soil, resulting in runoff, characterized by flood channels and wadis. Physical, inorganic crusts have been extensively investigated because of their negative impact on arid agricultural land. What little moisture does remain in the soil undergoes excessive evapotranspiration. Deserts bordering coastal lands derive most of their moisture from moist onshore breezes. This moisture evaporates from the soil leaving behind high concentrations of NaCl. Wind also affects the ecosystem of desert areas, where strong air currents in desert regions cause wind erosion and the phenomena of moving dunes (Wiggs et al., 1995, 2001). The scarce plant distribution in deserts provides little protection from wind-soil erosion forces. In addition to uprooting and sometimes covering pioneering plants, wind-driven soil transport reduces the nutrient content of soils. In New Mexico, aeolian transport of soil was shown to reduce organic carbon and nitrogen in the ground by 25% (Junran et al., 2007). This was attributed to the fact that most photosynthetic and nitrogen fixation occurs in the top few millimeters of soil (Garcia-Pichel and Belnap, 2001). This erosion and hampered nutrient availability makes colonization all but impossible for most species of flora and fauna. Diel temperature fluctuations in arid environments also present a unique hurdle for pioneering organisms to overcome. Extremely high daytime temperatures can cause lethal desiccation in plant

0140-1963/$ e see front matter Ó 2013 Published by Elsevier Ltd. http://dx.doi.org/10.1016/j.jaridenv.2013.11.004

Please cite this article in press as: Powell, J.T., et al., Desert crust microorganisms, their environment, and human health, Journal of Arid Environments (2013), http://dx.doi.org/10.1016/j.jaridenv.2013.11.004

2

J.T. Powell et al. / Journal of Arid Environments xxx (2013) 1e7

species. After dusk, near or below freezing temperatures can freeze and lyse plant cells. Hot deserts typically experience diel temperature ranges from 0 C to 37 C, while cold deserts such as those in Greenland, can fluctuate from as little as 0 C to 4 C. The Hopq Desert in China experiences minimum temperatures below 30 C and high temperatures above 40 C (Wang et al., 2013). 2. Prokaryotic organisms in desert environments 2.1. Hypolithic Hypolithic bacterial communities have been studied less extensively than the photosynthetic cyanobacterial ones, which dominate this ecosystem. The abiotic factors that determine the composition and activity of hypolithic bacterial communities are available liquid water derived from rainfall and fog as well as salinity (Azua-Bustos et al., 2011; Pointing et al., 2009; WarrenRhodes et al., 2006). Studies performed in the Atacama desert, Chile, show that both soil and hypolithic heterotrophs are positively correlated to soil moisture from rainfall and thus more abundant in wetter sites along a 11,500 m2 precipitation gradient (Navarro-González et al., 2003; Warren-Rhodes et al., 2006). Based on 16S rRNA-sequence diversity analysis, hypolithic communities unlike soil communities, were comprised primarily of Acidobacteria, alpha, beta and gamma sub-classes of the Proteobacteria and were co-extracted with cyanobacterial colonizers. Stomeo et al. (2013) working with samples collected in the Namib desert, spanning the Atlantic coasts of Angola, Namibia and South Africa, showed that rainfall-moisture has a different effect on both soil and hypolithic communities than fog-moisture. A higher number of Operational Taxonomic Units (OTU) derived from terminal restriction length polymorphisms (T-RFLP) of the 16S rRNA gene were observed in hypolithic communities of rainfalldominated sites than those from fog-dominated sites. In contrast, soil communities were not influenced by the climate as they had a similar number of OTUs in both regimes. Also, the genetic fingerprints derived from soil communities revealed greater overall variation than those derived from the hypolithic communities. Makhalanyane et al. (2013) concluded that the noted variations suggest soil and hypolithic communities do not develop in isolation from one another but have cross recruitment. 2.2. Desert crusts Obligate heterotrophic bacterial communities are important components of the consortium of organisms that make up the desert crusts. Their colonization on the crust is subsequent to the pioneering cyanobacteria who are the dominant primary producers contributing to nitrogen and carbon fixation. Investigation of the spatial patterns of heterotrophic bacterial communities at the micro-scale revealed a crust maturity-dependent distribution (Evans and Johansen, 1999). In pioneering desert crusts in the Colorado Plateau, communities were most abundant in the immediate sub-surface (1e2 mm), whereas in the more welldeveloped pigmented crusts the highest abundance was observed on the surface (0e1 mm) (Garcia-Pichel et al., 2003). Other studies performed at the centimeter to kilometer scale failed to observe such vertical stratification of the heterotrophic communities, yet the range of total viable counts are comparable and decline with depth (3.1 102e3.6 107 CFU/g of soil) (Bolton et al., 1993; Kuske et al., 2002; Skujins, 1984). The soil texture of desert crusts is also a determining factor in the total number of microorganisms they can support. The lowest numbers are found in exposed or compacted crusts and un-crusted soil followed by silt-surface crusts. Clay crusts support the highest

numbers of bacteria owing to their ability to hold more moisture and organic matter within the pore space where microbial life exists (Gallardo and Schlesinger, 1995; Garcia-Pichel et al., 2003; Saxton and Rawls, 2006; Skujins, 1984). Phylogenetic analyses using culture-independent methods indicate that the majority of 16S rRNA sequences amplified from desert crust soils belong to cyanobacteria. In cases where crust samples originate from hyper-arid sites, they constitute up to 80% of the total sequenced community (Abed et al., 2010; Zaady et al., 2010). The bacterial populations uniformly belong to the phyla of Bacteroidetes, Proteobacteria, Deinococcus-Thermus and Gemmatimonadetes with the exception of the delta-Proteobacterial Myxobacteria only found in desert crust samples from Oman, and the phylum Actinobacteria detected only in the Sonoran desert and Colorado Plateau (Gundlapally and Garcia-Pichel, 2006; Nagy et al., 2005). 3. Prokaryotic organisms in dust storms originating from desert environments Microbes attached to mineral dust or other airborne particles are transported over long distances (Griffin, 2007). Whitman et al. (1998) demonstrated that as many as 109 bacterial cells may be contained in one gram of desert dust, yet the abiotic factors that influence their population numbers, diversity and distribution are still not well understood. In general, concentrations of airborne microbes are higher during dust events, as compared to background conditions, and bacterial populations outweigh those of fungi (Choi et al., 1997; Griffin et al., 2001, 2003; Kellogg et al., 2004; Prospero et al., 2005). Survival of microorganisms in the atmosphere is dependent on the same abiotic factors as their survival in desert environments, namely, the ability to withstand desiccation, extreme temperature fluctuations, oxygen and nutrient limitation and exposure to UV radiation (Alan and Harrison, 2004; Imshenetsky et al., 1978). According to the available literature, the best predictors of both the total number of bacteria and culturable bacteria in the atmosphere are air temperature and wind speed (Bovallius et al., 1978; Harrison et al., 2005; Mouli et al., 2005). Estimates of total bacterial concentrations in the atmosphere are the lowest in the desert ecosystem (1.6 102e3.8 104 CFU/m3) and comparable to those of the sea air (Burrows et al., 2009; Lighthart and Shaffer, 1994). Dust identified bacteria are phylogenetically affiliated with a plethora of genera belonging to the phyla of Gram-positive Firmicutes and Actinobacteria and the Gram-negative Proteobacteria. The majority of the bacteria isolated from African dust events over the Caribbean were Gram-positive spore-formers belonging to the genera Bacillus and Microbacterium (Griffin et al., 2001, 2003; Prospero et al., 2005). Perfumo and Marchant (2010) isolated thermophilic species of Geobacillus from African desert dust over Turkey and Greece and Hua et al. (2007) isolated halotolerant strains of Staphylococcus and Bacillus and of the Gram-negative Halomonas from Asian desert dust events in Japan. Finally, Leski et al. (2011) detected the presence of potential human pathogens in airborne samples collected from locations in Iraq and Kuwait by using a newly-designed high-density resequencing microarray. Genera identified include the Gram-positive Mycobacterium, Clostridium and Bacillus and the Gram-negative intracellular parasites Brucella and Coxiella. 4. Cyanobacteria desert adaptations Cyanobacteria are so well adapted to the extremes of living conditions that they have been suggested for pioneering life on Mars (Friedmann and Ocampo-Friedmann, 1995). Indeed, fossils



suggest that cyanobacteria were present billions of years ago (Schopf, 1993) and contributed to the oxygen atmosphere present today (Berkner and Marshall, 1965). While cyanobacteria can be difficult to classify based on physiology and morphology alone, two general types have been classified, based upon their tolerance to UV light. UV-sensitive cyanobacteria colonize beneath the soil surface and are mainly composed of Microcoleus. Rather than be exposed to UV radiation and wind scouring, UV sensitive cyanobacteria lie desiccated beneath the soil surface until activated by moisture to glide to the surface. They return to their subsurface position before once again desiccating (Belnap, 2006; Wang et al., 2013). Similarly, some cyanobacterial species are capable of living inside the pores of rocks. These endoliths take advantage of the same protections and opportunity provided by living beneath sand (Fig. 1). In the current review, we focus on UV-tolerant cyanobacteria which in desert environments, are principally composed of Scytonema and Nostoc species. These cyanobacteria live on the soil surface and possess direct adaptive mechanisms to the desert environment, particularly to temperature fluctuations and wet/dry cycles. They have developed the ability to reversibly activate their metabolism, limiting photosynthesis and growth to wet periods when the cells are rehydrated. During hot, dry periods, the cells enter into a quiescent state. Although photosystems I and II (PSI, PSII) are damaged during high light and dryness, in vitro studies have shown that PS I and PSII are self-repaired and operational within minutes of the cell’s rehydration (Harel et al., 2004). This ability of the cyanobacterial cell to recover from photoinhibition almost immediately after rehydration is paramount to their survival. The cyanobacteria on desert surfaces also protect their photosynthetic mechanisms and genetic material with UV-protective pigments. Cyanobacteria developed protective pigments during a time when UV exposure was far greater than present. In terms of ozone protection, ancient taxa of cyanobacteria survived early

3

environmental times when atmospheric oxygen was 105 that of its present concentration (Berkner and Marshall, 1965). Cyanobacteria evolved pigments, scytonemin and mycosporine-like amino acids (MAA; Fig. 2), which absorb potentially lethal doses of UV radiation (UVR; Proteau et al., 1993 and Soule et al., 2009). These pigments are so effective that they are currently being evaluated for use as a more effective sunscreen for human use. Scytonemin and its derivatives occur at varying frequency in cyanobacterial species. In stratiform, epithilic crust mats, the heavily pigmented cyanobacteria on top protect deeper microorganisms. Extracellular polysaccharides appear to contribute to UV radiation protection as well. MAA deposited in the polysaccharide layer acts as a biological sunscreen. The MAA structures include a central cyclohexenone ring, which is thought to block UV radiation and absorb free radicals (Rossia et al., 2012). Despite the cyanobacteria’s impressive adaptations, they remain vulnerable to anthropogenic disturbance. Recovery times for cyanobacteria disrupted by human activities are considered to be measured in centuries (Belnap, 2003). 5. Positive aspects of cyanobacteria in desert environments 5.1. Fertilization of desert substrate Cyanobacterial crusts are the primary producers in the arid environments they inhabit. The ability of these microorganisms to fix nitrogen and fertilize the desert substrates they occupy is important in nutrient-poor desert landscapes. Since vascular plants cannot use atmospheric nitrogen gas, they rely on bacterial species to fix nitrogen gas (N2) into more useful biological nitrogen sources, such as ammonia (NHþ 4 ) (Harper and Marble, 1988). Developing seeds below the soil surface depend on this nitrogen. Fortunately for desert plants, cyanobacteria include diazotrophic species capable of fixing N2, although their capacity to do this relies on photosynthesis for ATP and electron donor compounds (Paul and Clark, 1996). In addition to the need for light, cyanobacteria also require moisture to fix nitrogen, as they are metabolically inactive during periods of desiccation. Furthermore, when light and moisture are available, cyanobacterial nitrogen fixation is affected by temperature, usually occurring between 5 C and 30 C (Belnap, 2001a). It should also be noted that cyanobacteria are capable of solubilising phosphate compounds, increasing the concentration of soil phosphorus and plant phosphorus uptake (Rodríguez and Fraga, 1999). Their role in increasing both nitrogen and phosphorus in arid soils has attracted agricultural research attention (Wu et al., 2013), suggesting that artificially developed soil crusts could inoculate target soil. 5.2. Prevention of wind erosion and water loss

Fig. 1. Examples of cyanobacteria in Qatar desert: A) Hypoliths on overturned rock; B) Stratified cyanobacteria crust from the Inland Sea; C) Rehydrated surface cyanobacteria crust; D) Endoliths inside quartz.

Cyanobacteria also stabilize desert substrates and enhance moisture retention, combating wind erosion and evapotranspiration, respectively. The efficiency of intact cyanobacterial soil crust to decrease wind erosion is similar to that of physical soil crusts and rock material. Extracellular polysaccharides combine with surrounding sand grains to form extensive and resilient matrices that resist erosion. The role of such polysaccharides is paramount as demonstrated by the wind stability of chemically killed soil crusts in which the polysaccharide matrix is left intact (Williams et al., 1995). The large matrices are more aerodynamic than the singular grains of sand and their resistance increases proportionally to the size of the aggregate matrix. That is however, until these crusts are disrupted by anthropogenic activity, at which point they disintegrate and lose much of their erosion resistance (Belnap, 2001b).


4


Fig. 2. Examples of UV protective pigments found in cyanobacteria: A) Scytonemin; B) Shinorine; C) Porphyra-334.

The role of cyanobacterial crusts in arid soil water retention is complex. Semi-arid, loamy soil environments enjoy increased infiltration and retention of water when biological soil crusts are present. In these climates, cyanobacteria prevent physical surface sealing (Morin and Benyamini, 1977). In the arid desert climate, where sandy soils naturally experience even infiltration, cyanobacterial crusts seem to decrease infiltration and cause runoff much like physical soil crust. This runoff, in turn causes redistribution of water resources, imparting diversity to the soil systems within the desert ecosystem (Yair, 2001). It is, however, very important to note that previously desiccated cyanobacteria absorb a great deal of water prior to saturation before facilitating runoff. Campbell (1979) and Wang et al. (1981) report cyanobacterial sheaths may absorb up to 12 times their dry weight and increase their volume up to 10 times (Yair, 2001).

involve acute respiratory distress, however, systemic chronic illness has also been linked to fungal spore exposure. Mycotoxins produced by these fungi have been linked to liver, kidney, gastrointestinal, heart, central nervous system and immune system complications and illness (Piecková and Jesenká, 1999). Growth and toxin production in these fungi are linked to moisture and heat availability, which would suggest that these species might be able to produce these same toxins in water saturated desert cyanobacterial crusts. However, little research has been conducted in characterizing fungal toxin production or human exposure models in desert environments.

6. Toxin production by microorganisms and prokaryotes in desert environments

Although cyanobacteria occur in a wide variety of environments throughout the world, including terrestrial, poles, and deserts, they are most commonly associated with aquatic environments. This association with aquatic environments is largely due to both their overall abundance and their affect on the aesthetics and quality of water used for recreation and drinking. While the production of geosmin and methylisoborneol by cyanobacteria is known to adversely affect the taste and odour of drinking water (Metcalf and Codd, 2012; Metcalf et al., 2013), it is their production of highly toxic compounds which results in animal and human health poisonings and deaths (Codd et al., 1999). The range of animal species that have been affected by cyanobacterial toxins is vast, from camels and cattle, to bats and bird species, such as the Lesser Flamingo, which feeds on cyanobacteria as a major food source in African Rift Valley lakes (Metcalf and Codd, 2012). Human health

While the viral and bacterial constituents of desert soil have been extensively studied due to their presence in dust storms, little is known about toxin-producing microorganisms other than cyanobacteria. Vastly diverse communities of fungi have been discovered living within biological soil crusts. These fungi most likely play a role in organic plant material breakdown in a symbiotic or mutualistic relationship with plant species. Taxa of fungal species in cyanobacterial crusts in Utah and Wyoming included Aspergillus spp., Fusarium spp. and Cladosporium spp. (States et al., 2001). The presence of these fungal species and their adverse health effects in human domiciles has been extensively studied (Cabral, 2010; Hedayati et al., 2010). Although most health effects

7. Negative aspects of cyanobacteria in desert environments 7.1. Toxin production



incidents attributed to cyanobacterial toxins are generally thought to be rare and the incidence of mortality is generally less than for animal species affected by cyanobacterial toxins. However, human deaths have occurred, most notably at a hemodialysis clinic at Caruaru, Brazil, where inadequately treated water containing cyanobacterial toxins, was the cause of patient mortality and illness (Carmichael et al., 2001; Codd et al., 1999). The toxic compounds produced by cyanobacteria have a variety of structures, modes of action and effects in mammalian systems. The most commonly reported cyanobacterial toxins are the cyclic peptide hepatotoxins; the microcystins and nodularins. The seven (microcystins) and five (nodularins) amino acid cyclic compounds are potent inhibitors of protein phosphatases and phosphoprotein phosphatases (Hastie et al., 2005). In large enough doses, death can occur by hypovolemic shock due to the destruction of the liver, and in combination with tumour initiators, microcystins may act as tumour promoters. Other hepatotoxic compounds include the cylindrospermopsins, cyclic guanidine alkaloids which have been shown to be produced by cyanobacterial genera including Cylindrospermopsis, Anabaena and Aphanizomenon. They act by inhibiting protein translation as demonstrated in the rabbit reticulocyte lysate assay (Froscio et al., 2001), and are also considered to be carcinogenic (Humpage, 2008). Other alkaloid toxins produced by cyanobacteria include the anatoxins, anatoxin-a and anatoxin-a(S). Anatoxin-a is a highly toxic compound which acts as an acetylcholine mimic, causing death by paralysis at high enough doses and is commonly found to be produced by Phormidium species. Anatoxin-a(S) although with a similar name, can be produced by Anabaena and has a completely different mode of action. The structure and action is that of an organophosphate, similar to organophosphorus pesticides, which inhibit acetylcholine esterases resulting in paralysis and death at sufficient concentration (Metcalf and Codd, 2012). Cyanobacteria have also been shown to be capable of producing saxitoxins, common shellfish poisoning toxins associated with marine dinoflagellate blooms and contaminated shellfish (Llewellyn, 2009). Saxitoxins are extremely potent natural products, with their major mode of action acting through the inhibition of sodium channels. In high enough doses, death can occur in minutes due to paralysis and respiratory arrest (Metcalf and Codd, 2012). Although a large number of cyanotoxins are known for their rapid and acute toxicity, neurotoxic amino acids, shown to be produced by cyanobacteria, have gained interest due to their connection to long-term human neurodegenerative diseases (Cox

5

et al., 2003; Murch et al., 2004). In particular, b-N-methylamino(BMAA) has been identified in 95% of cyanobacterial strains tested (Cox et al., 2005; Esterhuizen and Downing, 2008) and also occurs in the brains of patients who died of Amyotrophic Lateral Sclerosis (ALS), Alzheimer’s and Parkinson’s disease (Bradley and Mash, 2009; Murch et al., 2004; Pablo et al., 2009). A characteristic shared by all Gram-negative bacteria is their capacity to produce lipopolysaccharide (LPS; Drews and Weckesser, 1982). LPS is considered to be produced by all cyanobacteria and reports of gastrointestinal upset have been reported after consumption of drinking water associated with cyanobacteria (Codd et al., 1999). Although cyanobacteria are major components of desert environments, so far, little research has considered the occurrence and fate of cyanobacterial toxins in these environments. Where terrestrial desert material has been analysed, BMAA, microcystins and anatoxin-a(S) (Fig. 3) have been identified in cyanobacterial crust material from Qatar, confirming that human and animal exposure in desert environments may have occurred (Cox et al., 2009; Metcalf et al., 2012; Richer et al., in this volume). L-alanine

7.2. Exposure routes Much of the research concerning exposure routes to cyanobacterial toxins has developed from our understanding of exposure through aquatic media (Codd et al.,1999, 2005). The most commonly considered exposure route is through the consumption of contaminated drinking water or contaminated foods such as fish and shellfish (Brand et al., 2010; Jonasson et al., 2010). Crops can also be contaminated through accidental exposure as blooms of cyanobacteria can occur and grow within tanks used for crop-spray irrigation (Codd et al.,1999). As shown by the deaths of haemodialysis patients in Caruaru, Brazil, intravenous administration of cyanotoxins through inadequately treated water can lead to fatalities. In addition to ingestion, certain practices such as showering and cooking with lake water, and water sports such as kayaking and wind surfing can result in exposure to cyanotoxins with potential adverse health outcomes if a cyanobacterial bloom is present in the area (Codd et al., 2005, 1999). Due to the current perception that cyanotoxin exposure is most likely to occur through aquatic media, the regulations and allocation factors used to set guidelines have largely overlooked nonaquatic environments where cyanobacteria (and toxins) may occur. The prevalence of deserts and cyanobacteria are well known and the limited information available suggests that cyanotoxins

Fig. 3. Examples of cyanotoxins identified in desert crusts (Cox et al., 2009; Metcalf et al., 2012) (clockwise): A) BMAA; B) Microcystin; C) Anatoxin-a(S).


6


may be present in these environments (Cox et al., 2009; Metcalf et al., 2012). Therefore, the potential that alternative exposure routes may exist in non-aquatic desert environments is something that has so far not been extensively considered and further research is necessary to understand the contributions of the various exposure routes (See Richer et al., in this volume). In deserts, water resources are precious and where present, ponds have been shown to produce cyanobacterial blooms containing microcystins, BMAA, 2,4-diamino-butyric acid (DAB), and N-(2-aminoethyl)glycine (AEG) (Banack et al., 2012; Craighead et al., 2009; Mohamed et al., 2006). Furthermore, some agricultural practices such as crop irrigation do occur and it is possible that such waters may contain cyanotoxins, resulting in the potential for human exposure. However, a regular feature of deserts is the occurrence of dust storms, which can persist for days. As the coverage of cyanobacteria in the desert can be considerable (Richer et al., 2012), and as these dust storms are known to contain cyanobacteria (Griffin, 2007), it is therefore possible that cyanotoxins may be present in dust storms. The effects of continued exposure to dust containing cyanobacteria through inhalation in dust storms should not be overlooked and it is possible that inhalation of cyanobacteria through dust storms could lead to an elevated adverse health risk (Metcalf et al., 2012). The limited research to date on the presence and exposure routes of cyanobacterial toxins in desert environments suggests that further research is necessary to understand the risk associated with adverse human (and animal) health outcomes. Furthermore, adequate human health monitoring could help to elucidate the long-term human health impact of exposure to cyanobacterial toxins in desert environments. 8. Conclusions Desert environments are arguably among the most adverse places on terrestrial earth for life to exist. Nevertheless, desert biomes are expansive, composed of primeval species that have evolved elaborate adaptations. Desert crusts have survived via evolved mechanisms protecting them from freeze-thaw, extreme temperature fluctuations, desiccation, and ultra-violet radiation. While these cyanobacteria positively influence their environment as pioneer species, they also produce toxins that could be hazardous to human and animal health. Further characterization of these cyanobacterial toxins needs to be performed with an emphasis on routes of human exposure and possibilities to mitigate adverse health effects. Additionally, the possible potentiating role of other microbial and fungal toxins needs to be investigated. Research on cyanobacteria, microbes, and fungal species toxin production has been extensively conducted in other environments. Further research on these toxins needs to include desert environments, which are increasingly populated and used for agricultural and livestock grazing worldwide. The potential of deserts to expand with the threat from global climate change makes these studies increasingly urgent. Acknowledgements We wish to thank the Qatar National Research Fund (project NPRP 4-775-1-116) and the Charles Engelhard Foundation for funding this research. References Abed, R.M.M., Al Kharusi, S., Schramm, A., Michael, D., Robinson, M.D., 2010. Bacterial diversity, pigments and nitrogen fixation of biological desert crusts from the Sultanate of Oman. FEMS Microbiol. Ecol. 72, 418e428.

Alan, M.J., Harrison, R.M., 2004. The effects of meteorological factors on atmospheric bioaerosol concentrationsda review. Sci. Total Environ. 326, 151e180. Azua-Bustos, A., Gonzalez-Silva, C., Mancilla, R.A., Salas, L., Gomez-Silva, B., McKay, C.P., Vicuna, R., 2011. Hypolithic cyanobacteria supported mainly by fog in the coastal range of the Atacama Desert. Microb. Ecol. 61, 568e581. Banack, S.A., Metcalf, J.S., Jiang, L., Craighead, D., Ilag, L.L., Cox, P.A., 2012. Cyanobacteria produce N-(2-Aminoethyl)Glycine, a backbone for peptide nucleic acids which may have been the first genetic molecules for life on earth. PLoS ONE 7 (11), e49043. Belnap, J., 2001a. Factors influencing nitrogen fixation and nitrogen release in biological soil crusts. Ecol. Stud. 150, 241e261. Belnap, J., 2001b. Biological soil crusts and wind erosion. Ecol. Stud. 150, 339e347. Belnap, J., 2003. The world at your feet: desert biological soil crusts. Front. Ecol. Environ. 1, 181e189. Belnap, J., 2006. The potential roles of biological soil crusts in dryland hydrologic cycles. Hydrol. Process. 20, 3159e3178. Berkner, L.V., Marshall, L.C., 1965. On the origin and rise of oxygen concentration in the Earth’s atmosphere. J. Atmos. Sci. 22, 225e261. Bolton Jr., H., Smith, J.L., Link, S.O., 1993. Soil microbial biomass and activity of a disturbed and undisturbed shrub-steppe ecosystem. Soil Biol. Biochem. 25, 545e552. Bovallius, A., Bucht, B., Roffey, R., Anas, P., 1978. Three-year investigation of the natural airborne bacterial flora at four localities in Sweden. Appl. Environ. Microbiol. 35, 847e852. Bradley, W.G., Mash, D.C., 2009. Beyond Guam: the cyanobacteria/BMAA hypothesis of the cause of ALS and other neurodegenerative diseases. Amyotroph. Lateral Scler. 10 (S2), 7e20. Brand, L.E., Pablo, J., Compton, A., Hammerschlag, N., Mash, D.C., 2010. Cyanobacterial blooms and the occurrence of the neurotoxin, beta-N-methylamino-Lalanine (BMAA), in South Florida aquatic food webs. Harmful Algae 9, 620e635. Burrows, S.M., Elbert, W., Lawrence, M.G., Pöschl, U., 2009. Atmospheric bacteria in different ecosystems. Atmos. Chem. Phys. Discuss. 9, 10777e10827. Cabral, J., 2010. Can we use indoor fungi as bioindicators of indoor air quality? Historical perspectives and open questions. Sci. Total Environ. 408 (20), 4285e 4295. Campbell, S.E., 1979. Soil stabilization by prokaryotic desert crust. Implication for Precambrian land biota. Orig. Life 9, 335e348. Carmichael, W.W., Azevedo, S.M.F.O., An, J.S., Molica, P.J.R., Jochimsen, E.M., Lau, S., Rinehart, K.L., Shaw, G.R., Eaglesham, G.K., 2001. Human fatalities from cyanobacteria: chemical and biological evidence for cyanotoxins. Environ. Health Perspect. 109, 663e668. Choi, D., Park, Y., Oh, S., Yoon, H., Kim, J., Seo, W., Cha, S., 1997. Distribution of airborne microorganisms in yellow sands of Korea. J. Microbiol. 35, 1e9. Codd, G.A., Bell, S.G., Kaya, K., Ward, C.J., Beattie, K.A., Metcalf, J.S., 1999. Cyanobacterial toxins, exposure routes and human health. Eur. J. Phycol. 34, 405e415. Codd, G.A., Morrison, L.F., Metcalf, J.S., 2005. Cyanobacterial toxins: risk management for health protection. Toxicol. Appl. Pharmacol. 203, 264e272. Cox, P.A., Banack, S.A., Murch, S.J., 2003. Biogmagnification of cyanobacterial neurotoxins and neurodegenerative disease among the Chamorro people of Guam. Proc Natl. Acad. Sci. U. S. A. 100, 13380e13383. Cox, P.A., Banack, S.A., Murch, S.J., Rasmussen, U., Tien, G., Bidigare, R.R., Metcalf, J.S., Morrison, L.F., Codd, G.A., Bergman, B., 2005. Diverse taxa of cyanobacteria produce b-N-methylamino-L-alanine, a neurotoxic amino acid. Proc. Natl. Acad. Sci. U. S. A. 102, 5074e5078. Cox, P.A., Richer, R., Metcalf, J.S., Banack, S.A., Codd, G.A., Bradley, W.G., 2009. Cyanobacteria and BMAA exposure from desert dust: a possible link to sporadic ALS among Gulf War veterans. Amyotroph. Lateral Scler. 10 (S2), 109e117. Craighead, D., Metcalf, J.S., Banack, S.A., Amgalan, L., Reynolds, H.V., Batmunkh, M., 2009. Presence of the neurotoxic amino acids b-N-methylamino-L-alanine (BMAA) and 2,4-diamino-butyric acid (DAB) in shallow springs from the Gobi Desert. Amyotroph. Lateral Scler. 10 (S2), 96e100. Davila, A.F., Gómez-Silva, B., de los Rios, A., Ascaso, C., Olivares, H., McKay, C.P., Wierzchos, J., 2008. Facilitation of endolithic microbial survival in the hyperarid core of the Atacama Desert by mineral deliquescence. J. Geophys. Res. 113, G01028. Drews, G., Weckesser, J., 1982. Function, structure and composition of cell walls and external layers. In: Carr, N.G., Whitton, B.A. (Eds.), The Biology of Cyanobacteria. Blackwell Scientific Publications Ltd., Oxford, pp. 333e357. Esterhuizen, M., Downing, T.G., 2008. b-N-methylamino-L-alanine (BMAA) in novel South African Cyanobacterial isolates. Ecotoxicol. Environ. Saf. 71, 309e313. Evans, R.D., Johansen, J.R., 1999. Microbiotic crusts and ecosystem processes. Crit. Rev. Plant Sci. 18, 183e225. FAO Forest Resources Division, 1989. Arid Zone Forestry: a Guide for Field Technicians. FAO Conservation Guide no. 20. FAO Publications, Rome, Italy. Friedmann, E.I., Ocampo-Friedmann, R., 1995. A primitive cyanobacterium as pioneer microorganism for terraforming Mars. Adv. Space Res. 15, 243e246. Froscio, S.M., Humpage, A.R., Burcham, P.C., Falconer, I.R., 2001. Cell-free protein synthesis inhibition assay for the cyanobacterial toxin cylindrospermopsin. Environ. Toxicol. 16, 408e412. Gallardo, A., Schlesinger, W.H., 1995. Factors determining soil microbial biomass and nutrient immobilization in desert soils. Biogeochemistry 28, 55e68. Garcia-Pichel, F., Belnap, J., 2001. Small-scale environments and distribution of biological soil crusts. In: Belnap, J., Lange, O. (Eds.), Biological Soil Crusts: Structure, Function, and Management. Springer-Verlag, Berlin, pp. 193e201.


J.T. Powell et al. / Journal of Arid Environments xxx (2013) 1e7 Garcia-Pichel, F., Johnson, S.L., Youngkin, D., Belnap, J., 2003. Small-scale vertical distribution of bacterial biomass and diversity in biological soil crusts from arid lands in the Colorado plateau. Microb. Ecol. 46, 312e321. Griffin, D., Garrison, V., Herman, J., Shinn, E., 2001. African desert dust in the Caribbean atmosphere: microbiology and public health. Aerobiologia 17, 203e 213. Griffin, D., Kellogg, C., Garrison, V., Lisle, J., Borden, T., Shinn, E., 2003. Atmospheric microbiology in the northern Caribbean during African dust events. Aerobiologia 19, 143e157. Griffin, D.W., 2007. Atmospheric movement of microorganisms in clouds of desert dust and implications for human health. Clin. Microbiol. Rev. 20, 459e477. Gundlapally, S.R., Garcia-Pichel, F., 2006. The community and phylogenetic diversity of biological soil crusts in the Colorado Plateau studied by molecular fingerprinting and intensive cultivation. Microb. Ecol. 52, 345e357. Harel, Y., Ohad, T., Kaplan, A., 2004. Activation of photosynthesis and resistance to photoinhibition in cyanobacteria within biological desert crust. Plant Physiol. 136, 3070e3079. Harper, K.T., Marble, J.R., 1988. A role for nonvascular plants in management of arid and semiarid rangelands. In: Tueller, P.T. (Ed.), Vegetation Science Applications for Rangeland Analysis and Management. Kluwer Academdic Publishers, Dordrecht, pp. 135e169. Harrison, R., Jones, A., Biggins, P., Pomeroy, N., Cox, C., Kidd, S., Hobman, J., Brown, N., Beswick, A., 2005. Climate factors influencing bacterial count in background air samples. Int. J. Biometeorol. 49, 167e178. Hastie, C.J., Borthwick, E.B., Morrison, L.F., Codd, G.A., Cohen, P.T.W., 2005. Inhibition of several protein phosphatases by a non-covalently interacting microcystin and a novel cyanobacterial peptide, nostocyclin. Biochim. Biophys. Acta 1726, 187e193. Hedayati, M., Mayahi, S., Denning, D., 2010. A study on Aspergillus species in houses of asthmatic patients from Sari City, Iran and a brief review of the health effects of exposure to indoor Aspergillus. Environ. Monit. Assess. 168, 481e487. Hua, N.-P., Kobayashi, F., Iwasaka, Y., Shi, G.-Y., Naganuma, T., 2007. Detailed identification of desert-originated bacteria carried by Asian dust storms to Japan. Aerobiologia 23, 291e298. Humpage, A.R., 2008. Toxin types, toxicokinetics and toxicodynamics. Adv. Exp. Med. Biol. 619, 383e415. Imshenetsky, A.A., Lysenko, S.V., Kazakov, G.A., 1978. Upper boundary of the biosphere. Appl. Environ. Microbiol. 35, 1e5. Jonasson, S., Eriksson, J., Berntzon, L., Spá cil, Z., Ilag, L.L., Ronnevi, L.O., Rasmussen, U., Bergman, B., 2010. Transfer of a cyanobacterial neurotoxin within a temperate aquatic ecosystem suggests pathways for human exposure. Proc. Natl. Acad. Sci. U. S. A. 107, 9252e9257. Junran, L., Okin, G., Alvarez, L., Epstein, H., 2007. Quantitative effects of vegetation cover on wind erosion and soil nutrient loss in a desert grassland of southern New Mexico, USA. Biogeochemistry 85, 317e332. Kellogg, C., Griffin, D., Garrison, V., Peak, K., Royall, N., Smith, R., Shinn, E., 2004. Characterization of aerosolized bacteria and fungi from desert dust events in Mali, West Africa. Aerobiologia 20, 99e110. Kuske, C.R., Ticknor, L.O., Miller, M.E., Dunbar, J.M., Davis, J.A., Barns, S.M., Belnap, J., 2002. Comparison of soil bacterial communities in rhizospheres of three plant species and the interspaces in an arid grassland. Appl. Environ. Microbiol. 68, 1854e1863. Leski, T.A., Malanoski, A.P., Gregory, M.J., Lin, B., Stenger, D.A., 2011. Application of a broad-range resequencing array for detection of pathogens in desert dust samples from Kuwait and Iraq. Appl. Environ. Microbiol. 77, 4285e4292. Lighthart, B., Shaffer, B.T., 1994. Bacterial flux from chaparral into the atmosphere in mid-summer at a high desert location. Atmos. Environ. 28, 1267e1274. Llewellyn, L.E., 2009. Sodium channel inhibiting marine toxins. Prog. Mol. Subcell. Biol. 46, 67e97. Makhalanyane, T.P., Valverde, A., Lacap, D.C., Stephen, B., Pointing, S.B., Tuffin, M.I., Don, A., Cowan, D.A., 2013. Evidence of species recruitment and development of hot desert hypolithic communities. Environ. Microbiol. Reports 5, 219e224. Metcalf, J.S., Codd, G.A., 2012. Cyanotoxins. In: Whitton, B.A. (Ed.), Ecology of Cyanobacteria II: Their Diversity in Space and Time. Springer, Dordrecht, Germany, pp. 651e675. Metcalf, J.S., Richer, R., Cox, P.A., Codd, G.A., 2012. Cyanotoxins in desert environments may present a risk to human health. Sci. Total Environ. 421e422, 118e 123. Metcalf, J.S., Banack, S.A., Kotud, K., Krienitz, L., Codd, G.A., 2013. Amino acid neurotoxins in feathers of the Lesser Flamingo, Phoeniconaias minor. Chemosphere 90, 835e839. Mohamed, Z.A., El-Sharouny, H.M., Ali, W.S.F., 2006. Microcystin production in benthic mats of cyanobacteria in the Nile River and irrigation canals, Egypt. Toxicon 47, 584e590. Mouli, P., Mohan, S., Reddy, S., 2005. Assessment of microbial (bacteria) concentrations of ambient air at semi-arid urban region: influence of meteorological factors. Appl. Ecol. Environ. Res. 3, 139e149. Morin, J., Benyamini, Y., 1977. Rainfall infiltration into bare soils. Water Res. 13, 813e 817.

7

Murch, S.J., Cox, P.A., Banack, S.A., 2004. A mechanism for the slow release of biomagnified cyanobacterial neurotoxins and neurodegenerative disease in Guam. Proc. Natl. Acad. Sci. U. S. A. 101, 12228e12231. Nagy, M.L., Pérez, A., Garcia-Pichel, F., 2005. The prokaryotic diversity of biological soil crusts in the Sonoran Desert (Organ Pipe Cactus National Monument, AZ). Fems Microbiol. Ecol. 54, 233e245. Navarro-González, R., Rainey, F., Molina, P., Bagaley, D., Hollen, B., de la Rosa, J., Small, A., Quinn, R., Cáceres, L., Gomez-Silva, B., McKay, C.P., 2003. Mars-like soils in the Atacama Desert, Chile, and the dry limit of microbial life. Science 302, 933e1096. Pablo, J., Banack, S.A., Cox, P.A., Johnson, T.E., Papapetropoulos, S., Bradley, W.G., Buck, A., Mash, D.C., 2009. Cyanobacterial neurotoxin BMAA in ALS and Alzheimer’s disease. Acta Neurol. Scand. 120, 216e225. Paul, E.A., Clark, F.E., 1996. Soil Microbiology and Microchemistry. Academic Press, London. Perfumo, A., Marchant, R., 2010. Global transport of thermophilic bacteria in atmospheric dust. Environ. Microbiol. Reports 2, 333e339. Piecková, E., Jesenká, Z., 1999. Microscopic fungi in dwellings and their health implications in humans. Ann. Agric. Environ. Med. 6, 1e11. Pointing, S.B., Chan, Y., Lacap, D.C., Lau, M.C.Y., Jurgens, J.A., Farrell, R.L., 2009. Highly specialized microbial diversity in hyper-arid polar desert. Proc. Natl. Acad. Sci. U. S. A. 106, 19964e19969. Prospero, J., Blades, E., Mathison, G., Naidu, R., 2005. Interhemispheric transport of viable fungi and bacteria from Africa to the Caribbean with soil dust. Aerobiologia 21, 1e19. Proteau, P.J., Gerwick, W.H., Garcia-Pichel, F., Castenholz, R., 1993. The structure of scytonemin, an ultraviolet sunscreen pigment from the sheaths of cyanobacteria. Experientia 49, 825e829. Richer, R., Anchassi, D., El-Assaad, I., El-Matbouly, M., Ali, F., Makki, I., Metcalf, J.S., 2012. Variation in the coverage of biological soil crusts in the State of Qatar. J. Arid Environ. 78, 187e190. Richer, R., Banack, S.A., Metcalf, J.S., Cox, P.A., 2013. The persistence of cyanobacterial toxins in desert soils. J. Arid Environ. (in this volume). Rodríguez, H., Fraga, R., 1999. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv. 17, 319e339. Rossia, F., Michelettia, E., Brunob, L., Adhikaryc, S., Albertanob, P., De Philippisa, R., 2012. Characteristics and role of the exocellular polysaccharides produced by five cyanobacteria isolated from phototrophic biofilms growing on stone monument. Biofouling 28, 215e224. Saxton, K.E., Rawls, W.J., 2006. Soil water characteristic estimates by texture and organic matter for hydrologic solutions. Soil Sci. Soc. Am. J. 70, 1569e1578. Schopf, J.W., 1993. Microfossils of the early archean apex chert: new evidence of the antiquity of life. Science 260, 640e646. Skujins, J., 1984. Microbial ecology of desert soils. Adv. Microb. Ecol. 7, 49e91. Soule, T., Palmer, K., Gao1, Q., Potrafka1, R., Stout, V., Garcia-Pichel, F., 2009. A comparative genomics approach to understanding the biosynthesis of the sunscreen scytonemin in cyanobacteria. BMC Genomics 10, 336. States, J.S., Christensen, M., Kinter, C.L., 2001. Soil fungi as components of biological soil crusts. Ecol. Stud. 150, 155e166. Stomeo, F., Valverde, A., Pointing, S.B., McKay, C.P., Warren-Rhodes, K.A., Tuffin, M.I., Seely, M., Cowan, D.A., 2013. Hypolithic and soil microbial community assembly along an aridity gradient in the Namib Desert. Extremophiles 17, 329e337. Wang, F., Zhung, Z., Hu, Z., 1981. Nitrogen fixation by an edible terrestrial blue-green algae. In: Gibson, A.H., Newton, W.E. (Eds.), Current Perspectives in Nitrogen Fixation. Elsevier, Amsterdam, pp. 450e455. Wang, W., Wang, Y., Shu, X., Zhang, Q., 2013. Physiological responses of soil crustforming cyanobacteria to diurnal temperature variation. J. Basic Microbiol. 53, 72e80. Warren-Rhodes, K.A., Rhodes, K.L., Pointing, S.B., Ewing, S.A., Lacap, D.C., GómezSilva, B., Amundson, R., Friedmann, E.I., McKay, C.P., 2006. Hypolithic cyanobacteria, dry limit of photosynthesis, and microbial ecology in the hyperarid Atacama Desert. Microb. Ecol. 52, 389e398. Whitman, W., Coleman, D., Wiebe, W., 1998. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. U. S. A. 95, 6578e6583. Wiggs, G.F.S., Thomas, D.S.G., Bullard, J.E., Livingstone, I., 1995. Dune mobility and vegetation cover in the Southwest Kalahari Desert. Earth Surf. Process. Landf. 20, 515e529. Wiggs, G.F.S., 2001. Desert dune processes and dynamics. Prog. Phys. Geogr. 25, 53e79. Williams, J.D., Dobrowolski, J.P., West, N.E., Gillette, D.A., 1995. Microphytic crust influence on wind erosion. Trans. Am. Soc. Agric. Eng. 38, 131e137. Wu, Y., Rao, B., Wu, P., Liu, Y., Li, G., Li, D., 2013. Development of artificially induced biological soil crusts in fields and their effects on top soil. Plant Soil. http:// dx.doi.org/10.1007/s11104-013-1611-6. Yair, A., 2001. Effects of biological soil crusts on water redistribution in the Negev Desert, Israel: a case study in longitudinal dunes. Ecol. Stud. 150, 303e314. Zaady, E., Ben-David, E.A., Sher, Y., Tzirkin, R., Ali Nejidat, A., 2010. Inferring biological soil crust successional stage using combined PLFA, DGGE, physical and biophysiological analyses. Soil Biol. Biochem. 42, 842e849.
