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Snow moulds in polar environments
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Snow moulds in polar environments Motoaki TOJOa,*, Kevin K. NEWSHAMb a
Graduate School of Life and Environmental Sciences, Osaka Prefecture University, Sakai, Osaka 599-8531, Japan British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, United Kingdom
b
article info
abstract
Article history:
Snow moulds are fungi and fungal-like microbes that occur frequently as pathogens of
Received 29 September 2011
moss and vascular plant species in the Arctic and Antarctic, chiefly in maritime areas with
Revision received 30 November 2011
permanent snow cover for several months of each year. Here, we review the environments
Accepted 20 December 2011
inhabited by polar snow moulds, their distribution and the macroscopic features of
Available online 17 February 2012
infections, such as the sclerotia that form on the leaves of higher plants, or the more
Corresponding editor:
frequently encountered concentric rings found in moss stands. The microscopic features of
Lynne Boddy
infections are described, as are the taxa of snow moulds found in polar habitats, such as the ascomycetes Thyronectria antarctica var. hyperantarctica and Sclerotinia borealis, the
Keywords:
basidiomycete Typhula ishikariensis and the oomycete Pythium. Recent research, also
Antarctic
reviewed here, indicates that a heterothallic species of Pythium apparently has a bipolar
Arctic
distribution. The adaptations of snow moulds to polar environments, such as their growth
Ascomycetes
at low temperatures, are covered, as are avenues for future research on these microbes.
Basidiomycetes
ª 2012 Elsevier Ltd and The British Mycological Society. All rights reserved.
Bipolar distribution Oomycetes Opportunistic parasites Psychrophiles Psychrotrophs Pythium
Introduction Snow moulds are fungi and fungal-like micro-organisms that are pathogens of plants in cool temperate environments (Iriki et al. 2001; Hoshino et al. 2009). They are essentially opportunistic parasites that attack their hosts under snow cover when plant resistance is lowered by interrupted photosynthesis and the eventual exhaustion of reserve materials (Nakajima & Abe 1994; Hoshino et al. 2009). Snow moulds occur not only in cool temperate zones but are also frequent in Antarctic and Arctic habitats, where they cause distinctive infection patterns in moss and higher plant tissues (Longton 1973; Fenton 1983; Hoshino et al. 2003, 2004, 2006a; Bridge et al. 2008). In this review, we describe the environments inhabited by polar snow moulds, the
macro- and microscopic features of infections, the different taxa causing snow mould infections in polar habitats, and their adaptations and responses to low temperatures. Finally, we suggest avenues for future research on these microbes.
Environments inhabited by polar snow moulds Snow moulds are frequently encountered in polar regions in stands of plants in damp or wet habitats (Longton 1973). They usually occur in maritime areas on level ground at the bases of cliffs where snowdrifts form during spring, or in rills and moist stream beds (Hoshino et al. 2001a), although they have also been recorded in high alpine areas of Greenland and
* Corresponding author. Tel.: þ81 72 254 9411; fax: þ81 72 254 9918. E-mail address: [email protected] (M. Tojo). 1754-5048/$ e see front matter ª 2012 Elsevier Ltd and The British Mycological Society. All rights reserved. doi:10.1016/j.funeco.2012.01.003
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Spitsbergen (Wilson 1951). Snow moulds typically infect plants that are covered with snow and ice for several months of each year. As noted in many studies, sub-nival environments are relatively stable in temperature. For example, at Barrow (71 170 N, 156 460 W), on the shores of the Arctic Ocean, the temperature of plants under snow of 260 mm depth was constant at 7 C in late spring, until meltwater percolated through the snow shortly before complete snowmelt (Tieszen 1974). At Rothera Point on Adelaide Island close to the western Antarctic Peninsula (67 340 S, 68 070 W), at which infections caused by snow moulds occur in the moss Sanionia uncinata, the temperatures of plants under snow and ice during spring and autumn have been measured at between 0 C and 7 C, with temperatures only falling to 20 C and occasionally 30 C during winter (Newsham 2010). At Signy Island (60 420 S, 45 350 W) in the South Orkneys in the maritime Antarctic, at which snow moulds have been frequently reported (Longton 1973; Fenton 1983; Bridge et al. 2008), temperatures of S. uncinata under >500 mm of snow cover have been similarly measured at between 1 C and 6 C during spring and autumn (Davey et al. 1992). During the summer, however, the temperatures of plants at Rothera Point and at Signy Island can frequently reach 15e20 C at solar noon under cloudless skies, and routinely fall to freezing point at night (Davey et al. 1992; Newsham 2010). Thus, although the sub-nival environment provides a relatively thermally stable habitat for snow moulds, these microbes are adapted to survive wide variations in temperature in polar habitats after emergence from snow and ice cover. Plant tissues under snow in polar habitats are frozen and desiccated (Wasley et al. 2006), but water availability will rise rapidly as ice- and snow-melt occurs. Plants, in which photosynthesis has been interrupted for several months, and from which reserve materials have been exhausted, thus frequently emerge from snow and ice cover with water contents of several hundred percent (Newsham, unpubl. data), favouring the development of snow moulds in their tissues. This is consistent with the view that the development of snow mould infections, which occur frequently in hydrophilous species of moss in both Arctic and Antarctic habitats (Fenton 1983; Hoshino et al. 1999; Yamazaki et al. 2011), is associated with water availability (Tronsmo et al. 2001). However, precipitation in polar habitats is typically low, with annual precipitation of <350 mm per annum in southern maritime Antarctic habitats, the majority of which falls as snow (Smith 1984). Similarly, in Kongsfjorden (79 570 N, 11 290 E) on Spitsbergen in the high Arctic, at which snow moulds occur in colonies of S. uncinata, annual precipitation is 200e300 mm water equivalents per annum (Fleming et al. 1997), and daily rainfall only exceeds 5 mm on 15e20 d each year (Tojo & Nishitani 2005). Thus, unless fed by permanent sources of fresh water, plants can rapidly become desiccated after emergence from snow and ice-cover, presenting a further challenge to the survival of snow moulds.
Distribution and macroscopic features Snow mould infections are frequent throughout the Arctic and the maritime and sub-Antarctic (Fig 1). Some snow moulds, such as Typhula ishikariensis (speckled snow mould), T. incarnata (grey snow mould) and Sclerotinia borealis (snow scald) form sclerotia
M. Tojo, K.K. Newsham
Fig 1 e Locations at which snow mould infections have been recorded in the Arctic (top) and Antarctic (bottom). Open circles mark the positions at which sclerotial infections, caused by Typhula spp. and Sclerotinia borealis, have been recorded, and filled circles mark the positions of ring infections. Data from Wilson (1951), Ekstrand (1955), Jamalainen (1957), Lebeau & Logsdon (1958), Hawksworth (1973), Longton (1973), Arsvoll (1975), Kristinsson & Gudleifsson (1976), Ridley et al. (1979), Fenton (1983), Greenfield (1983), Smith (1982, 1994), Matsumoto & Tronsmo (1995), Hoshino et al. (1997, 1999, 2000, 2001a, 2001b, 2002, 2003, 2004, 2006a, 2006b); Shiryayev (2004, 2006, 2008), Tojo & Nishitani (2005), Bridge et al. (2008) and Yamazaki et al. (2011). Note that the numerous records of Typhula spp. infections recorded by Jamalainen (1957) in southern Finland are not shown.
Snow moulds in polar environments
measuring 0.6e5.5 mm diameter on higher plant tissues, and typically grasses such as Poa hartzii and Phleum pratense, on Spitsbergen and Greenland and in Alaska, northern Norway, Finland, Sweden, Iceland and Russia (Ekstrand 1955; Jamalainen 1957; Lebeau & Logsdon 1958; Kristinsson & Gudleifsson 1976, Matsumoto & Tronsmo 1995; Hoshino et al. 1997, 2003, 2004, 2006b; Shiryayev 2004, 2006, 2008). Sclerotial infections appear to be restricted to the Arctic (Fig 1). Because Typhula spp. and S. borealis are psychrophiles (see Adaptations of snow moulds to low temperatures, below), their sclerotia, which are tolerant to
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drought, remain dormant in summer (Hoshino et al. 2003, 2009). In contrast to temperate habitats, in which some snow moulds develop fruiting structures that produce spores, which form an infective stage, the myceliogenic germination of S. borealis from sclerotia, leading to disease, has been reported in Alaska (McBeath 1988). Infections caused by Typhula spp. and S. borealis usually cause only moderate bleaching and dieback of plant tissues unless the duration of snow cover is prolonged. In addition to the sclerotial infections caused by Typhula spp. and S. borealis, ring infections, typically in monospecific stands of
Fig 2 e Occurrence of radial infection patterns caused by unidentified, non-sclerotial sterile basidiomycetes on moss colonies at King George Island, Antarctica. (A) radial infection patterns in colonies of mosses just after snowmelt. (B) dense wefts of hyphae on Sanionia uncinata, and (C) Bryum sp. and Ceratodon sp., (D) white moribund stems and leaves of S. uncinata associated with radially spreading fungal infection and (E) hypha with clamp connection formed on white moribund stems and leaves of S. uncinata. Bar 10 mm (photos by M. Tojo).
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bryophytes, are often formed by snow moulds in both Arctic and Antarctic habitats (Fig 1). These rings bear a superficial resemblance to those formed by the fairy ring mushroom (Marasmius oreades) in temperate grasslands (Fisher 1977). In broad terms, two forms of rings caused by snow moulds are found in polar regions. The first of these are full or partial rings of up to 200 mm in diameter, consisting of white bands of 2e15 (20) mm width (Longton 1973; Fig 2AeC). Such rings form in moist to wet stands of mosses, typically species of Brachythecium, Calliergon (h Warnstorfia), Ceratodon, Dicranoweisia (h Hymenoloma) and Sanionia. Infections have been recorded on South Georgia, Candlemas Island in the South Sandwich Islands, King George Island in the South Shetland Islands, and Deception, Avian, Adelaide and the Refuge islands, each off the western Antarctic Peninsula (Longton 1973; Smith 1982, 1994), but they are most probably present throughout the maritime and sub-Antarctic (Fig 1). Observations indicate that they are infrequent in the arid coastal regions of Greater Antarctica (Hoshino et al. 2001a; Fig 1). In the Arctic, they have been recorded in stands of bryophytes such as S. uncinata, Bryum cryophyllum and Tortula ruralis on Spitsbergen, Greenland, Ellesmere Island and King George Island (Longton 1973; Tojo, unpubl. obs.). Adjacent rings can often merge together, forming intricate patterns on moss carpets, but concentric rings are rarely formed in these infections (Fig 2AeC). Inside the ring of white shoots, moss tissues are depressed and sometimes brown in colour, reverting to green in the centre of the ring as the moss tissues recover from infection (see Microscopic features, below). The growth rates of the rings have been estimated at 3e6 mm month1, with up to 25 mm expansion in a 4-month growing season at Signy Island in the Maritime Antarctic (Longton 1973). The other form of ring occurring in bryophyte stands in polar habitats usually consists of a series of concentric or partial circles, or occasionally linear infections, which are usually darkly pigmented. Such rings have been reported on moss species such as Racomitrium canescens var. ericoides on Jan Mayen and Spitsbergen in the Arctic and Chorisodontium aciphyllum, S. uncinata and Calliergidium austrostramineum (h Warnstorfia fontinaliopsis) on Signy Island in the South Orkneys (Wilson 1951; Ridley et al. 1979; Fenton 1983). The moss in the concentric rings is brown or greenish-brown in colour, surrounded by rings of pale green, and is blackened in the centre of the rings. The annual rate of spread of the rings at Jan Mayen is estimated to be 50e100 mm yr1 (Wilson 1951). The rings form after snowmelt at 5e10 mm beyond the front from the previous year, with two to three rings (and up to six) being formed during each summer. Infected moss in the rings turns brown, and, if it is killed, then black. The radial advance of the fungus usually results in a series of concentric rings, but if the ring is broken, then the infection spreads in the shape of an arc, and occasionally as a continuous straight front. Based upon a mean rate of spread of c. 80 mm yr1, rings at Signy Island were estimated to be c. 15e20 yr old, with a straight infection front of 10 m length being reported (Fenton 1983).
M. Tojo, K.K. Newsham
moss S. uncinata in the maritime Antarctic. Once infection is established in a carpet, hyphae spread outwards by forming dense wefts on the surface of actively growing apical parts of plants, where they penetrate the stem and leaf tissues of virtually every shoot. At about the same time, a brown discolouration develops locally on the stems, and the leaf protoplasts begin to disintegrate. Later, almost complete breakdown of the protoplasts results in the upper parts of the infected plants turning white in colour (Fig 2D). The lower brown stem region appears to act as necrotic tissue, preventing the spread of the fungus down the shoot. Intracellular septate hyphae of 2.0e3.7 mm diameter are observed in almost every cell in the damaged parts of leaves, with hyphae usually lying parallel to the long axis of cells and showing constrictions where they pass through cell walls. Intracellular hyphae are also found in stem cells, particularly in the region below the stem apex. As the hyphae of the fungus continue to spread outwards, shoots in the centre of the original area of attack regenerate by the production of laterals, resulting in the circular pattern observed on moss carpets. Similar features were noted in darkly-pigmented rings formed by snow moulds in R. canescens var. ericoides on Jan Mayen by Wilson (1951). Shoots of the moss in the outer ring were the most heavily infected with hyphae, with the majority of cells containing hyphae bearing clamp connections and the hyphae lying parallel with the long axes of the cells. Almost all cytoplasmic content was lost from cells that were infected. The nitrogen content of moss tissues fell from 70 p.p.m. in uninfected stems to 40 p.p.m. in the outer and inner rings, which was thought to be associated with leaching of the element from the tissues following decomposition (Wilson 1951). Asci are frequently encountered in the upper shoots of mosses infected with ascomycetous snow moulds in the maritime Antarctic (Longton 1973). It is possible that these structures are able to survive sub-nival environments during the winter and then lead to subsequent colonisation of fresh moss tissues in the spring. In snow mould infections caused by oomycetes (see below), globose sporangia and sporangium-like structures are found on and in damaged tissues. There is also anecdotal evidence of chlamydospore formation in tissues, suggesting that these structures may be used to survive long periods under snow and ice during polar winters, again leading to the colonisation of fresh tissues after the emergence of plants from snow and ice in the spring (Bridge et al. 2008).
Taxa of snow moulds in polar environments Many different species of fungi appear to be associated with snow mould infections in polar vegetation. It appears likely that the ring infections described above are usually not caused by any one species of snow mould, but that a suite of fungi are involved, since often more than one fungus has been encountered in a ring, or system of rings (e.g. Fenton 1983).
Ascomycetes
Microscopic features Longton (1973) described the processes by which snow moulds, causing white rings of up to 200 mm in diameter, develop in the
At several islands in the maritime Antarctic, T. antarctica var. hyperantarctica, Coleroa turfosorum, Bryosphaeria megaspora, Epibryon chorisodontii and an unidentified Plectomycete have
Snow moulds in polar environments
been recorded in both types of ring infection described above in the Distribution and macroscopic features section (Hawksworth 1973; Longton 1973; Fenton 1983). However, it is unclear if these fungi were the primary pathogens responsible for the formation of the rings. At Barentsburg (78 040 N, 14 140 E) on Spitsbergen in the high Arctic, Microdochium nivale and S. borealis, both of which are known as snow moulds on grasses in temperate regions (Smith 1986; Hoshino et al. 2009), have been recorded on P. hartzii (Hoshino et al. 2003, 2006b). Although usually regarded as a saprotroph, Trichoderma polysporum (teleomorph: Hypocrea pachybasioides), which is common in Arctic regions, colonises the moss S. uncinata, causing asymptomatic infections (Yamazaki et al. 2011).
Basidiomycetes The speckled snow mould fungus T. ishikariensis, and usually strains belonging to T. ishikariensis group III, has been commonly recorded in the Arctic, for example on Greenland, northern Norway, Iceland, Lapland, Sweden and Spitsbergen (Hoshino et al. 1997, 2003, 2004, 2006b), and is particularly common in areas with >5 months snow cover each year (Hoshino et al. 2009). Studies have recorded hyphae forming clamp connections in the tissues of plants infected by snow moulds (Wilson 1951; Fig 2E). Similar basidiomycete snow moulds lacking a conidial and known sexual stage have been reported in western Canada (Broadfoot & Cormack 1941; Smith 1975; Gaudet & Bhalla 1988). The smut fungus Microbotryum bistortarum has also been shown to have deleterious effects on the growth and survival of Polygonum viviparum under snow cover in the Arctic (Tojo & Nishitani 2005). Systemic smuts usually have a minimal effect on the survival of adult plants in temperate regions, but a reduction of resistance to winter injury may enhance the damage by the smut fungus (Tojo & Nishitani 2005), a view supported by Gaudet & Chen (1988), who reported that plants infected by pathogens are more susceptible to low temperature-related winter injury than healthy ones.
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monophyletic group have also been consistently recorded from both polar regions, including Adelaide, Humble and King George islands in the Antarctic (Hughes et al. 2003; Bridge et al. 2008; Arenz & Blanchette 2011; Yu & Hur, unpubl.) and Spitsbergen, Greenland, alpine Norway and Baffin Island in the Arctic (Hoshino et al. 2000, 2006a; Tojo et al. 2001; Tojo et al. unpubl.). This oomycete, which is frequently isolated from brown discoloured moss and underlying soils, causes brown discolouration of stem leaves of mosses in wet areas. Recent research indicates that it may have a bipolar distribution (Fig 3), with the internal transcribed spacer (ITS) regions of isolates from the Antarctic and Arctic being on average 97.5 % similar to each other. They are 90e93 % similar to those of Pythium canariense, P. iwayamai, P. paddicum, P. okanoganense and P. violae, which each belong to Pythium clade G described vesque & de Cock (2004), but cluster separately from by Le these sequences, indicating that they form a distinct subclade (Fig 3). Pythium iwayamai, P. paddicum and P. okanoganense are the most common members of Pythium clade G to cause snow mould infections on winter cereals and grasses in Japan, the United States and European regions of Russia (Lipps & Bruehl 1978; Petrov 1983; Takamatsu & Takenaka 2001; Masumoto et al. 2009), and are considered to be the most aggressive snow moulds in the clade (Takamatsu 1989). Although Pythium clade G is thought to contain more snow mould pathogens than the other clades of the genus,
Zygomycetes The only report of a zygomycete snow mould in polar regions is that of Greenfield (1983), who observed a species of Rhizopus to be pathogenic on Bryum antarcticum at Cape Bird (77 130 S 166 540 E) on Ross Island in the continental Antarctic.
Oomycetes There are many records of oomycetes forming snow mould infections in polar environments. These oomycetes typically belong to the genus Pythium, which are frequently associated with the white ring infections (see Distribution and macroscopic features, above) on mosses such as S. uncinata, Aulacomnium palustre, Calliergon stramineum and Tomenthypnum nitens in Arctic habitats (Hoshino et al. 2001b). These oomycetes usually belong to the Pythium HS group (Hoshino et al. 2000, 2001b), but Pythium ultimum var. ultimum has also been recorded as a snow mould pathogen at several locations on Spitsbergen (Hoshino et al. 1999). However, isolates of an undescribed heterothallic Pythium sp. belonging to the same
Fig 3 e Consensus maximum likelihood tree of internal transcribed spacer region sequences of Pythium isolates from polar regions and those belonging to clade G, vesque & de Cock (2004). Bootstrap values described by Le are shown at major branching points. Outgroup is vesque & de Phytophthora avicenniae AY598668 (after Le Cock 2004). Modified from Bridge et al. (2008).
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M. Tojo, K.K. Newsham
evaluations of the members of the other clades as causal agents of snow mould infections are limited (Lipps & Bruehl 1978; Takamatsu 1989).
Adaptations of snow moulds to low temperatures Snow moulds in polar environments are apparently psychrophilic (cold-loving) or psychrotrophic (cold-tolerant) organisms. Psychrophiles are capable of growth at temperatures below freezing point, but are unable to grow at >20 C, whereas psychrotrophs are able to tolerate temperatures above 20 C. Sclerotinia borealis has a minimum growth temperature of 5 C, an optimum growth temperature of 5 C, and a maximum growth temperature of <20 C, and is thus classed as a psychrophile (Hoshino et al. 2003). Also classed as a psychrophile is T. ishikariensis: group I and III isolates of this fungus from Finnmark in northern Norway grow at 5 C, have optimum growth temperatures of 10 C and 4 C, respectively, and neither grow at 25 C (Fig 4). Isolates from group III have better tolerance to subzero temperatures than those from group I (Fig 4), corroborating data showing that members of the former group tend to inhabit colder environments (Hoshino et al. 1998). In contrast, most Pythium snow moulds from polar environments appear to be psychrotrophs. Pythium isolates from Longyearbyen (78 120 N, 15 360 E) and Barentsburg on Spitsbergen and from King George Island (62 130 S; 58 580 W) in the Antarctic grow at between 0 C and 10 C, which is consistent with the ability of Pythium to infect stems and leaves of S. uncinata and to cause discolouration of tissues at 5 C in in vitro inoculation tests (Tojo, unpubl.), but the optimum growth temperatures for these isolates are at 20 C or 25 C, and they are thus psychrotolerant (Fig 4). However, at >15 C, polar isolates of Pythium do not grow as rapidly as an isolate from Japan (Fig 4), indicating that they are better adapted to growth at low temperatures. Antifreeze proteins, which bind to ice crystals and prevent their expansion, are not synthesised by Pythium spp., accounting for the poor, or lack of, growth of these oomycetes at temperatures at or below freezing point (Fig 4). It has been found that although freezing destroys the hyphae of Pythium spp. and causes their mycelia to deform (Hoshino et al. 2002), the process breaks the dormancy of oospores (Tojo, unpubl.). A similar phenomenon has been found in P. iwayamai, the most common oomycete snow mould in Japan and the United States, which has highly freeze-tolerant oospores but mycelia that do not grow at 1 C (Takamatsu 1989; Hoshino et al. 2010). In contrast, basidiomycete snow moulds such as T. ishikariensis synthesise antifreeze proteins and are able to grow at subzero temperatures (Fig 4), since the cytosol remains unfrozen below freezing point (Hoshino et al. 1998). This ability has been ascribed to the production of a 30 kDa protein by the fungus (Hoshino et al. 1998). Typhula ishikariensis also synthesises a range of plant cell wall degrading enzymes such as cellulase, hemicellulase, polygalacturonase and xylanase that are active at low temperatures (Hoshino et al. 2009). Other snow mould fungi similarly synthesise enzymes that are active at low temperatures, such as polygalacturonase, which is active in isolates of T. polysporum from Spitsbergen at 0 C (Yamazaki
Fig 4 e Colony extension rates at different temperatures of group I and III Typhula ishikariensis isolates from Finnmark in northern Norway (top) and Pythium spp. isolates from Japan, Barentsburg and Longyearbyen on Spitsbergen in the Arctic, and King George Island in the Antarctic (bottom). Note that the y-axes are differently scaled. Modified from Hoshino et al. (1997, 2001a, 2001b).
et al. 2011). Snow mould fungi are also thought to alter the composition of their cell membranes in order to maintain their fluidity, with, for example, M. nivale increasing the amount of polyunsaturated fatty acids in its membranes at low temperatures (Istokovics et al. 1998).
Conclusions and future research Snow mould infections in polar environments are caused chiefly by ascomycetes, basidiomycetes and oomycetes, with those caused by zygomycetes being much less frequent. In
Snow moulds in polar environments
Arctic environments, infections caused by S. borealis and T. ishikariensis are found in the tissues of higher plants, and typically grasses. However, the most common type of snow mould infection in both the Arctic and Antarctic is the concentric or partial rings that form in stands of moss species, particularly in maritime areas with freely available water during summer and permanent snow cover for several months of each year. Although Pythium spp. are frequently recorded in these ring infections, several ascomycetes and sterile basidiomycetes have also been found in them, and so the identity of the primary pathogen in such infections remains unknown. Recent research indicates that a heterothallic species of Pythium, which is often associated with ring infections, appears to have a bipolar distribution. It is plausible that other snow moulds may similarly have bipolar distributions, particularly those caused by ascomycetes, spores of which remain viable after long-distance dispersal (Pady & Kapica 1953; Pady & Kelly 1954; Kubicek et al. 2008), but studies have yet to examine this possibility. Polar regions are currently warming at rapid rates, with the western Antarctic Peninsula, northern Greenland and northern North America being amongst the most rapidly warming regions on Earth (Hansen et al. 2006; Turner et al. 2009). In addition to rapid rises in air temperature, there are likely to be consequent changes to water availability in these regions, with, for example, increases in snow accumulation and precipitation having been recorded on the western Antarctic Peninsula in recent decades (Turner et al. 2005; Thomas et al. 2008). Such changes, coupled with higher air temperatures, are likely to lead to increased water availability as snow and ice melt in warmer environments. How such changes will influence snow moulds remains to be seen, but it is clear that there are likely to be changes in the frequencies of infections caused by snow moulds, since climatic factors, notably temperature and water availability, strongly influence the growth of snow moulds in both temperate and polar habitats (Nakajima & Abe 1994; Iriki et al. 2001; Hoshino et al. 1997, 2002, 2009). Research into the responses to climate change of these microbes, which can have substantial effects on plant fitness in the natural environment, is hence warranted.
Acknowledgements This study was supported by the Japan Society for the Promotion of Science by grant-in-aid for scientific research nos. 19510033, 23510032 and 23247012 (to MT), and by the Natural Environment Research Council (to KKN). Dr. Tamotsu Hoshino gave valuable information. Peter Fretwell kindly drew Fig 1 and two anonymous reviewers provided helpful comments.
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Hoshino T, Tojo M, Yumoto I, 2006a. Blight of moss caused by Pythium sp. in Greenland. Meddelelser on Groenland, Serie: Biocience 56: 95e98. Hoshino T, Saito I, Yumoto I, Tronsmo AM, 2006b. New findings of snow mold fungi from Greenland. Meddelelser on Groenland, Serie: Biocience 56: 89e94. Hoshino T, Xiao N, Tkachenko OB, 2009. Cold adaptation in the phytopathogenic fungi causing snow moulds. Mycoscience 50: 26e38. Hoshino T, Terami F, Takachenko OB, Tojo M, Matsumoto N, 2010. Mycelial growth of the snow mold fungus, Sclerotinia borealis, improved at low water potentials: an adaptation to frozen environment. Mycoscience 51: 98e103. Hughes KA, Lawley B, Newsham KK, 2003. Solar UV-B radiation inhibits the growth of Antarctic terrestrial fungi. Applied and Environmental Microbiology 69: 1488e1491. Iriki N, Gaudet DA, Tronsmo AM, Matsumoto N, Yoshida M, Nishimune A, 2001. Low Temperature Plant-microbe Interactions Under Snow. Hokkaido National Agricultural Experimental Station, Sapporo. Istokovics A, Morita N, Izumi K, Hoshino T, Yumoto I, Sawada MT, Ishizaki K, Okuyama H, 1998. Neutral lipids, phospholipids, and a betaine lipid of the snow mould fungus Microdochium nivale. Canadian Journal of Microbiology 44: 1051e1059. Jamalainen EA, 1957. Overwintering of Gramineae-plants and parasitic fungi. Journal of the Scientific Agricultural Society of Finland 29: 75e81. Kristinsson H, Gudleifsson BE, 1976. The activity of lowtemperature fungi under the snow cover in Iceland. Acta Botanica Islandica 4: 44e57. Kubicek CP, Komon-Zelazowska M, Druzhinina IS, 2008. Fungal genus Hypocrea/ Trichoderma: from barcodes to biodiversity. Journal of Zhejiang University-Science B 9: 753e763. Lebeau JB, Logsdon CE, 1958. Snow mold of forage crops in Alaska and Yukon. Phytopathology 48: 148e150. vesque CA, de Cock AWAM, 2004. Molecular phylogeny and Le taxonomy of the genus Pythium. Mycological Research 108: 1363e1383. Lipps PE, Bruehl GW, 1978. Snow rot of winter wheat in Washington. Phytopathology 68: 1120e1127. Longton RE, 1973. The occurrence of radial infection patterns in colonies of polar bryophytes. British Antarctic Survey Bulletin 32: 41e49. Masumoto S, Shigyo T, Tojo M, 2009. Pythium snow blight of Kentucky bluegrass turf in a golf course in Hokkaido, Japan. Journal of Japanese Society of Turfgrass Science 38: 33e36. Matsumoto N, Tronsmo AM, 1995. Population structure of Typhula ishikariensis in meadows and pastures in Norway. Acta Agriculturae Scandinavica, Section B, Soil and Plant Sciences 45: 197e201. McBeath JH, 1988. Sclerotia myceliogenic germination and pathogenicity of Sclerotinia borealis. In: 5th International Congress of Plant Pathology, Kyoto, p. 201. Nakajima T, Abe J, 1994. Development of resistance to Microdochium nivale in winter wheat during autumn and decline of the resistance under snow. Canadian Journal of Botany 72: 1211e1215. Newsham KK, 2010. The biology and ecology of the liverwort Cephaloziella varians in Antarctica. Antarctic Science 22: 131e143. Pady SM, Kapica L, 1953. Air-borne fungi in the Arctic and other parts of Canada. Canadian Journal of Botany 31: 309e323. Pady SM, Kelly CD, 1954. Aerobiological studies of fungi and bacteria over the Atlantic Ocean. Canadian Journal of Botany 32: 202e212. Petrov VF, 1983. Pathogenic microflora of root growth in perennial grasses in Khibiny. Bulletin of Applied Botany, Genetics and Plant Breeding 82: 38e45. Ridley M, Gillow C, Perkins D, Ogilvie J, 1979. Oxford University Expedition to Svalbard, 1978, vol. 29e72. Bulletin of the Oxford University Exploration Club. New Series, Commemoration.
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Snow moulds in polar environments Motoaki TOJOa,*, Kevin K. NEWSHAMb a
Graduate School of Life and Environmental Sciences, Osaka Prefecture University, Sakai, Osaka 599-8531, Japan British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, United Kingdom
b
article info
abstract
Article history:
Snow moulds are fungi and fungal-like microbes that occur frequently as pathogens of
Received 29 September 2011
moss and vascular plant species in the Arctic and Antarctic, chiefly in maritime areas with
Revision received 30 November 2011
permanent snow cover for several months of each year. Here, we review the environments
Accepted 20 December 2011
inhabited by polar snow moulds, their distribution and the macroscopic features of
Available online 17 February 2012
infections, such as the sclerotia that form on the leaves of higher plants, or the more
Corresponding editor:
frequently encountered concentric rings found in moss stands. The microscopic features of
Lynne Boddy
infections are described, as are the taxa of snow moulds found in polar habitats, such as the ascomycetes Thyronectria antarctica var. hyperantarctica and Sclerotinia borealis, the
Keywords:
basidiomycete Typhula ishikariensis and the oomycete Pythium. Recent research, also
Antarctic
reviewed here, indicates that a heterothallic species of Pythium apparently has a bipolar
Arctic
distribution. The adaptations of snow moulds to polar environments, such as their growth
Ascomycetes
at low temperatures, are covered, as are avenues for future research on these microbes.
Basidiomycetes
ª 2012 Elsevier Ltd and The British Mycological Society. All rights reserved.
Bipolar distribution Oomycetes Opportunistic parasites Psychrophiles Psychrotrophs Pythium
Introduction Snow moulds are fungi and fungal-like micro-organisms that are pathogens of plants in cool temperate environments (Iriki et al. 2001; Hoshino et al. 2009). They are essentially opportunistic parasites that attack their hosts under snow cover when plant resistance is lowered by interrupted photosynthesis and the eventual exhaustion of reserve materials (Nakajima & Abe 1994; Hoshino et al. 2009). Snow moulds occur not only in cool temperate zones but are also frequent in Antarctic and Arctic habitats, where they cause distinctive infection patterns in moss and higher plant tissues (Longton 1973; Fenton 1983; Hoshino et al. 2003, 2004, 2006a; Bridge et al. 2008). In this review, we describe the environments inhabited by polar snow moulds, the
macro- and microscopic features of infections, the different taxa causing snow mould infections in polar habitats, and their adaptations and responses to low temperatures. Finally, we suggest avenues for future research on these microbes.
Environments inhabited by polar snow moulds Snow moulds are frequently encountered in polar regions in stands of plants in damp or wet habitats (Longton 1973). They usually occur in maritime areas on level ground at the bases of cliffs where snowdrifts form during spring, or in rills and moist stream beds (Hoshino et al. 2001a), although they have also been recorded in high alpine areas of Greenland and
* Corresponding author. Tel.: þ81 72 254 9411; fax: þ81 72 254 9918. E-mail address: [email protected] (M. Tojo). 1754-5048/$ e see front matter ª 2012 Elsevier Ltd and The British Mycological Society. All rights reserved. doi:10.1016/j.funeco.2012.01.003
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Spitsbergen (Wilson 1951). Snow moulds typically infect plants that are covered with snow and ice for several months of each year. As noted in many studies, sub-nival environments are relatively stable in temperature. For example, at Barrow (71 170 N, 156 460 W), on the shores of the Arctic Ocean, the temperature of plants under snow of 260 mm depth was constant at 7 C in late spring, until meltwater percolated through the snow shortly before complete snowmelt (Tieszen 1974). At Rothera Point on Adelaide Island close to the western Antarctic Peninsula (67 340 S, 68 070 W), at which infections caused by snow moulds occur in the moss Sanionia uncinata, the temperatures of plants under snow and ice during spring and autumn have been measured at between 0 C and 7 C, with temperatures only falling to 20 C and occasionally 30 C during winter (Newsham 2010). At Signy Island (60 420 S, 45 350 W) in the South Orkneys in the maritime Antarctic, at which snow moulds have been frequently reported (Longton 1973; Fenton 1983; Bridge et al. 2008), temperatures of S. uncinata under >500 mm of snow cover have been similarly measured at between 1 C and 6 C during spring and autumn (Davey et al. 1992). During the summer, however, the temperatures of plants at Rothera Point and at Signy Island can frequently reach 15e20 C at solar noon under cloudless skies, and routinely fall to freezing point at night (Davey et al. 1992; Newsham 2010). Thus, although the sub-nival environment provides a relatively thermally stable habitat for snow moulds, these microbes are adapted to survive wide variations in temperature in polar habitats after emergence from snow and ice cover. Plant tissues under snow in polar habitats are frozen and desiccated (Wasley et al. 2006), but water availability will rise rapidly as ice- and snow-melt occurs. Plants, in which photosynthesis has been interrupted for several months, and from which reserve materials have been exhausted, thus frequently emerge from snow and ice cover with water contents of several hundred percent (Newsham, unpubl. data), favouring the development of snow moulds in their tissues. This is consistent with the view that the development of snow mould infections, which occur frequently in hydrophilous species of moss in both Arctic and Antarctic habitats (Fenton 1983; Hoshino et al. 1999; Yamazaki et al. 2011), is associated with water availability (Tronsmo et al. 2001). However, precipitation in polar habitats is typically low, with annual precipitation of <350 mm per annum in southern maritime Antarctic habitats, the majority of which falls as snow (Smith 1984). Similarly, in Kongsfjorden (79 570 N, 11 290 E) on Spitsbergen in the high Arctic, at which snow moulds occur in colonies of S. uncinata, annual precipitation is 200e300 mm water equivalents per annum (Fleming et al. 1997), and daily rainfall only exceeds 5 mm on 15e20 d each year (Tojo & Nishitani 2005). Thus, unless fed by permanent sources of fresh water, plants can rapidly become desiccated after emergence from snow and ice-cover, presenting a further challenge to the survival of snow moulds.
Distribution and macroscopic features Snow mould infections are frequent throughout the Arctic and the maritime and sub-Antarctic (Fig 1). Some snow moulds, such as Typhula ishikariensis (speckled snow mould), T. incarnata (grey snow mould) and Sclerotinia borealis (snow scald) form sclerotia
M. Tojo, K.K. Newsham
Fig 1 e Locations at which snow mould infections have been recorded in the Arctic (top) and Antarctic (bottom). Open circles mark the positions at which sclerotial infections, caused by Typhula spp. and Sclerotinia borealis, have been recorded, and filled circles mark the positions of ring infections. Data from Wilson (1951), Ekstrand (1955), Jamalainen (1957), Lebeau & Logsdon (1958), Hawksworth (1973), Longton (1973), Arsvoll (1975), Kristinsson & Gudleifsson (1976), Ridley et al. (1979), Fenton (1983), Greenfield (1983), Smith (1982, 1994), Matsumoto & Tronsmo (1995), Hoshino et al. (1997, 1999, 2000, 2001a, 2001b, 2002, 2003, 2004, 2006a, 2006b); Shiryayev (2004, 2006, 2008), Tojo & Nishitani (2005), Bridge et al. (2008) and Yamazaki et al. (2011). Note that the numerous records of Typhula spp. infections recorded by Jamalainen (1957) in southern Finland are not shown.
Snow moulds in polar environments
measuring 0.6e5.5 mm diameter on higher plant tissues, and typically grasses such as Poa hartzii and Phleum pratense, on Spitsbergen and Greenland and in Alaska, northern Norway, Finland, Sweden, Iceland and Russia (Ekstrand 1955; Jamalainen 1957; Lebeau & Logsdon 1958; Kristinsson & Gudleifsson 1976, Matsumoto & Tronsmo 1995; Hoshino et al. 1997, 2003, 2004, 2006b; Shiryayev 2004, 2006, 2008). Sclerotial infections appear to be restricted to the Arctic (Fig 1). Because Typhula spp. and S. borealis are psychrophiles (see Adaptations of snow moulds to low temperatures, below), their sclerotia, which are tolerant to
397
drought, remain dormant in summer (Hoshino et al. 2003, 2009). In contrast to temperate habitats, in which some snow moulds develop fruiting structures that produce spores, which form an infective stage, the myceliogenic germination of S. borealis from sclerotia, leading to disease, has been reported in Alaska (McBeath 1988). Infections caused by Typhula spp. and S. borealis usually cause only moderate bleaching and dieback of plant tissues unless the duration of snow cover is prolonged. In addition to the sclerotial infections caused by Typhula spp. and S. borealis, ring infections, typically in monospecific stands of
Fig 2 e Occurrence of radial infection patterns caused by unidentified, non-sclerotial sterile basidiomycetes on moss colonies at King George Island, Antarctica. (A) radial infection patterns in colonies of mosses just after snowmelt. (B) dense wefts of hyphae on Sanionia uncinata, and (C) Bryum sp. and Ceratodon sp., (D) white moribund stems and leaves of S. uncinata associated with radially spreading fungal infection and (E) hypha with clamp connection formed on white moribund stems and leaves of S. uncinata. Bar 10 mm (photos by M. Tojo).
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bryophytes, are often formed by snow moulds in both Arctic and Antarctic habitats (Fig 1). These rings bear a superficial resemblance to those formed by the fairy ring mushroom (Marasmius oreades) in temperate grasslands (Fisher 1977). In broad terms, two forms of rings caused by snow moulds are found in polar regions. The first of these are full or partial rings of up to 200 mm in diameter, consisting of white bands of 2e15 (20) mm width (Longton 1973; Fig 2AeC). Such rings form in moist to wet stands of mosses, typically species of Brachythecium, Calliergon (h Warnstorfia), Ceratodon, Dicranoweisia (h Hymenoloma) and Sanionia. Infections have been recorded on South Georgia, Candlemas Island in the South Sandwich Islands, King George Island in the South Shetland Islands, and Deception, Avian, Adelaide and the Refuge islands, each off the western Antarctic Peninsula (Longton 1973; Smith 1982, 1994), but they are most probably present throughout the maritime and sub-Antarctic (Fig 1). Observations indicate that they are infrequent in the arid coastal regions of Greater Antarctica (Hoshino et al. 2001a; Fig 1). In the Arctic, they have been recorded in stands of bryophytes such as S. uncinata, Bryum cryophyllum and Tortula ruralis on Spitsbergen, Greenland, Ellesmere Island and King George Island (Longton 1973; Tojo, unpubl. obs.). Adjacent rings can often merge together, forming intricate patterns on moss carpets, but concentric rings are rarely formed in these infections (Fig 2AeC). Inside the ring of white shoots, moss tissues are depressed and sometimes brown in colour, reverting to green in the centre of the ring as the moss tissues recover from infection (see Microscopic features, below). The growth rates of the rings have been estimated at 3e6 mm month1, with up to 25 mm expansion in a 4-month growing season at Signy Island in the Maritime Antarctic (Longton 1973). The other form of ring occurring in bryophyte stands in polar habitats usually consists of a series of concentric or partial circles, or occasionally linear infections, which are usually darkly pigmented. Such rings have been reported on moss species such as Racomitrium canescens var. ericoides on Jan Mayen and Spitsbergen in the Arctic and Chorisodontium aciphyllum, S. uncinata and Calliergidium austrostramineum (h Warnstorfia fontinaliopsis) on Signy Island in the South Orkneys (Wilson 1951; Ridley et al. 1979; Fenton 1983). The moss in the concentric rings is brown or greenish-brown in colour, surrounded by rings of pale green, and is blackened in the centre of the rings. The annual rate of spread of the rings at Jan Mayen is estimated to be 50e100 mm yr1 (Wilson 1951). The rings form after snowmelt at 5e10 mm beyond the front from the previous year, with two to three rings (and up to six) being formed during each summer. Infected moss in the rings turns brown, and, if it is killed, then black. The radial advance of the fungus usually results in a series of concentric rings, but if the ring is broken, then the infection spreads in the shape of an arc, and occasionally as a continuous straight front. Based upon a mean rate of spread of c. 80 mm yr1, rings at Signy Island were estimated to be c. 15e20 yr old, with a straight infection front of 10 m length being reported (Fenton 1983).
M. Tojo, K.K. Newsham
moss S. uncinata in the maritime Antarctic. Once infection is established in a carpet, hyphae spread outwards by forming dense wefts on the surface of actively growing apical parts of plants, where they penetrate the stem and leaf tissues of virtually every shoot. At about the same time, a brown discolouration develops locally on the stems, and the leaf protoplasts begin to disintegrate. Later, almost complete breakdown of the protoplasts results in the upper parts of the infected plants turning white in colour (Fig 2D). The lower brown stem region appears to act as necrotic tissue, preventing the spread of the fungus down the shoot. Intracellular septate hyphae of 2.0e3.7 mm diameter are observed in almost every cell in the damaged parts of leaves, with hyphae usually lying parallel to the long axis of cells and showing constrictions where they pass through cell walls. Intracellular hyphae are also found in stem cells, particularly in the region below the stem apex. As the hyphae of the fungus continue to spread outwards, shoots in the centre of the original area of attack regenerate by the production of laterals, resulting in the circular pattern observed on moss carpets. Similar features were noted in darkly-pigmented rings formed by snow moulds in R. canescens var. ericoides on Jan Mayen by Wilson (1951). Shoots of the moss in the outer ring were the most heavily infected with hyphae, with the majority of cells containing hyphae bearing clamp connections and the hyphae lying parallel with the long axes of the cells. Almost all cytoplasmic content was lost from cells that were infected. The nitrogen content of moss tissues fell from 70 p.p.m. in uninfected stems to 40 p.p.m. in the outer and inner rings, which was thought to be associated with leaching of the element from the tissues following decomposition (Wilson 1951). Asci are frequently encountered in the upper shoots of mosses infected with ascomycetous snow moulds in the maritime Antarctic (Longton 1973). It is possible that these structures are able to survive sub-nival environments during the winter and then lead to subsequent colonisation of fresh moss tissues in the spring. In snow mould infections caused by oomycetes (see below), globose sporangia and sporangium-like structures are found on and in damaged tissues. There is also anecdotal evidence of chlamydospore formation in tissues, suggesting that these structures may be used to survive long periods under snow and ice during polar winters, again leading to the colonisation of fresh tissues after the emergence of plants from snow and ice in the spring (Bridge et al. 2008).
Taxa of snow moulds in polar environments Many different species of fungi appear to be associated with snow mould infections in polar vegetation. It appears likely that the ring infections described above are usually not caused by any one species of snow mould, but that a suite of fungi are involved, since often more than one fungus has been encountered in a ring, or system of rings (e.g. Fenton 1983).
Ascomycetes
Microscopic features Longton (1973) described the processes by which snow moulds, causing white rings of up to 200 mm in diameter, develop in the
At several islands in the maritime Antarctic, T. antarctica var. hyperantarctica, Coleroa turfosorum, Bryosphaeria megaspora, Epibryon chorisodontii and an unidentified Plectomycete have
Snow moulds in polar environments
been recorded in both types of ring infection described above in the Distribution and macroscopic features section (Hawksworth 1973; Longton 1973; Fenton 1983). However, it is unclear if these fungi were the primary pathogens responsible for the formation of the rings. At Barentsburg (78 040 N, 14 140 E) on Spitsbergen in the high Arctic, Microdochium nivale and S. borealis, both of which are known as snow moulds on grasses in temperate regions (Smith 1986; Hoshino et al. 2009), have been recorded on P. hartzii (Hoshino et al. 2003, 2006b). Although usually regarded as a saprotroph, Trichoderma polysporum (teleomorph: Hypocrea pachybasioides), which is common in Arctic regions, colonises the moss S. uncinata, causing asymptomatic infections (Yamazaki et al. 2011).
Basidiomycetes The speckled snow mould fungus T. ishikariensis, and usually strains belonging to T. ishikariensis group III, has been commonly recorded in the Arctic, for example on Greenland, northern Norway, Iceland, Lapland, Sweden and Spitsbergen (Hoshino et al. 1997, 2003, 2004, 2006b), and is particularly common in areas with >5 months snow cover each year (Hoshino et al. 2009). Studies have recorded hyphae forming clamp connections in the tissues of plants infected by snow moulds (Wilson 1951; Fig 2E). Similar basidiomycete snow moulds lacking a conidial and known sexual stage have been reported in western Canada (Broadfoot & Cormack 1941; Smith 1975; Gaudet & Bhalla 1988). The smut fungus Microbotryum bistortarum has also been shown to have deleterious effects on the growth and survival of Polygonum viviparum under snow cover in the Arctic (Tojo & Nishitani 2005). Systemic smuts usually have a minimal effect on the survival of adult plants in temperate regions, but a reduction of resistance to winter injury may enhance the damage by the smut fungus (Tojo & Nishitani 2005), a view supported by Gaudet & Chen (1988), who reported that plants infected by pathogens are more susceptible to low temperature-related winter injury than healthy ones.
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monophyletic group have also been consistently recorded from both polar regions, including Adelaide, Humble and King George islands in the Antarctic (Hughes et al. 2003; Bridge et al. 2008; Arenz & Blanchette 2011; Yu & Hur, unpubl.) and Spitsbergen, Greenland, alpine Norway and Baffin Island in the Arctic (Hoshino et al. 2000, 2006a; Tojo et al. 2001; Tojo et al. unpubl.). This oomycete, which is frequently isolated from brown discoloured moss and underlying soils, causes brown discolouration of stem leaves of mosses in wet areas. Recent research indicates that it may have a bipolar distribution (Fig 3), with the internal transcribed spacer (ITS) regions of isolates from the Antarctic and Arctic being on average 97.5 % similar to each other. They are 90e93 % similar to those of Pythium canariense, P. iwayamai, P. paddicum, P. okanoganense and P. violae, which each belong to Pythium clade G described vesque & de Cock (2004), but cluster separately from by Le these sequences, indicating that they form a distinct subclade (Fig 3). Pythium iwayamai, P. paddicum and P. okanoganense are the most common members of Pythium clade G to cause snow mould infections on winter cereals and grasses in Japan, the United States and European regions of Russia (Lipps & Bruehl 1978; Petrov 1983; Takamatsu & Takenaka 2001; Masumoto et al. 2009), and are considered to be the most aggressive snow moulds in the clade (Takamatsu 1989). Although Pythium clade G is thought to contain more snow mould pathogens than the other clades of the genus,
Zygomycetes The only report of a zygomycete snow mould in polar regions is that of Greenfield (1983), who observed a species of Rhizopus to be pathogenic on Bryum antarcticum at Cape Bird (77 130 S 166 540 E) on Ross Island in the continental Antarctic.
Oomycetes There are many records of oomycetes forming snow mould infections in polar environments. These oomycetes typically belong to the genus Pythium, which are frequently associated with the white ring infections (see Distribution and macroscopic features, above) on mosses such as S. uncinata, Aulacomnium palustre, Calliergon stramineum and Tomenthypnum nitens in Arctic habitats (Hoshino et al. 2001b). These oomycetes usually belong to the Pythium HS group (Hoshino et al. 2000, 2001b), but Pythium ultimum var. ultimum has also been recorded as a snow mould pathogen at several locations on Spitsbergen (Hoshino et al. 1999). However, isolates of an undescribed heterothallic Pythium sp. belonging to the same
Fig 3 e Consensus maximum likelihood tree of internal transcribed spacer region sequences of Pythium isolates from polar regions and those belonging to clade G, vesque & de Cock (2004). Bootstrap values described by Le are shown at major branching points. Outgroup is vesque & de Phytophthora avicenniae AY598668 (after Le Cock 2004). Modified from Bridge et al. (2008).
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evaluations of the members of the other clades as causal agents of snow mould infections are limited (Lipps & Bruehl 1978; Takamatsu 1989).
Adaptations of snow moulds to low temperatures Snow moulds in polar environments are apparently psychrophilic (cold-loving) or psychrotrophic (cold-tolerant) organisms. Psychrophiles are capable of growth at temperatures below freezing point, but are unable to grow at >20 C, whereas psychrotrophs are able to tolerate temperatures above 20 C. Sclerotinia borealis has a minimum growth temperature of 5 C, an optimum growth temperature of 5 C, and a maximum growth temperature of <20 C, and is thus classed as a psychrophile (Hoshino et al. 2003). Also classed as a psychrophile is T. ishikariensis: group I and III isolates of this fungus from Finnmark in northern Norway grow at 5 C, have optimum growth temperatures of 10 C and 4 C, respectively, and neither grow at 25 C (Fig 4). Isolates from group III have better tolerance to subzero temperatures than those from group I (Fig 4), corroborating data showing that members of the former group tend to inhabit colder environments (Hoshino et al. 1998). In contrast, most Pythium snow moulds from polar environments appear to be psychrotrophs. Pythium isolates from Longyearbyen (78 120 N, 15 360 E) and Barentsburg on Spitsbergen and from King George Island (62 130 S; 58 580 W) in the Antarctic grow at between 0 C and 10 C, which is consistent with the ability of Pythium to infect stems and leaves of S. uncinata and to cause discolouration of tissues at 5 C in in vitro inoculation tests (Tojo, unpubl.), but the optimum growth temperatures for these isolates are at 20 C or 25 C, and they are thus psychrotolerant (Fig 4). However, at >15 C, polar isolates of Pythium do not grow as rapidly as an isolate from Japan (Fig 4), indicating that they are better adapted to growth at low temperatures. Antifreeze proteins, which bind to ice crystals and prevent their expansion, are not synthesised by Pythium spp., accounting for the poor, or lack of, growth of these oomycetes at temperatures at or below freezing point (Fig 4). It has been found that although freezing destroys the hyphae of Pythium spp. and causes their mycelia to deform (Hoshino et al. 2002), the process breaks the dormancy of oospores (Tojo, unpubl.). A similar phenomenon has been found in P. iwayamai, the most common oomycete snow mould in Japan and the United States, which has highly freeze-tolerant oospores but mycelia that do not grow at 1 C (Takamatsu 1989; Hoshino et al. 2010). In contrast, basidiomycete snow moulds such as T. ishikariensis synthesise antifreeze proteins and are able to grow at subzero temperatures (Fig 4), since the cytosol remains unfrozen below freezing point (Hoshino et al. 1998). This ability has been ascribed to the production of a 30 kDa protein by the fungus (Hoshino et al. 1998). Typhula ishikariensis also synthesises a range of plant cell wall degrading enzymes such as cellulase, hemicellulase, polygalacturonase and xylanase that are active at low temperatures (Hoshino et al. 2009). Other snow mould fungi similarly synthesise enzymes that are active at low temperatures, such as polygalacturonase, which is active in isolates of T. polysporum from Spitsbergen at 0 C (Yamazaki
Fig 4 e Colony extension rates at different temperatures of group I and III Typhula ishikariensis isolates from Finnmark in northern Norway (top) and Pythium spp. isolates from Japan, Barentsburg and Longyearbyen on Spitsbergen in the Arctic, and King George Island in the Antarctic (bottom). Note that the y-axes are differently scaled. Modified from Hoshino et al. (1997, 2001a, 2001b).
et al. 2011). Snow mould fungi are also thought to alter the composition of their cell membranes in order to maintain their fluidity, with, for example, M. nivale increasing the amount of polyunsaturated fatty acids in its membranes at low temperatures (Istokovics et al. 1998).
Conclusions and future research Snow mould infections in polar environments are caused chiefly by ascomycetes, basidiomycetes and oomycetes, with those caused by zygomycetes being much less frequent. In
Snow moulds in polar environments
Arctic environments, infections caused by S. borealis and T. ishikariensis are found in the tissues of higher plants, and typically grasses. However, the most common type of snow mould infection in both the Arctic and Antarctic is the concentric or partial rings that form in stands of moss species, particularly in maritime areas with freely available water during summer and permanent snow cover for several months of each year. Although Pythium spp. are frequently recorded in these ring infections, several ascomycetes and sterile basidiomycetes have also been found in them, and so the identity of the primary pathogen in such infections remains unknown. Recent research indicates that a heterothallic species of Pythium, which is often associated with ring infections, appears to have a bipolar distribution. It is plausible that other snow moulds may similarly have bipolar distributions, particularly those caused by ascomycetes, spores of which remain viable after long-distance dispersal (Pady & Kapica 1953; Pady & Kelly 1954; Kubicek et al. 2008), but studies have yet to examine this possibility. Polar regions are currently warming at rapid rates, with the western Antarctic Peninsula, northern Greenland and northern North America being amongst the most rapidly warming regions on Earth (Hansen et al. 2006; Turner et al. 2009). In addition to rapid rises in air temperature, there are likely to be consequent changes to water availability in these regions, with, for example, increases in snow accumulation and precipitation having been recorded on the western Antarctic Peninsula in recent decades (Turner et al. 2005; Thomas et al. 2008). Such changes, coupled with higher air temperatures, are likely to lead to increased water availability as snow and ice melt in warmer environments. How such changes will influence snow moulds remains to be seen, but it is clear that there are likely to be changes in the frequencies of infections caused by snow moulds, since climatic factors, notably temperature and water availability, strongly influence the growth of snow moulds in both temperate and polar habitats (Nakajima & Abe 1994; Iriki et al. 2001; Hoshino et al. 1997, 2002, 2009). Research into the responses to climate change of these microbes, which can have substantial effects on plant fitness in the natural environment, is hence warranted.
Acknowledgements This study was supported by the Japan Society for the Promotion of Science by grant-in-aid for scientific research nos. 19510033, 23510032 and 23247012 (to MT), and by the Natural Environment Research Council (to KKN). Dr. Tamotsu Hoshino gave valuable information. Peter Fretwell kindly drew Fig 1 and two anonymous reviewers provided helpful comments.
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