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Fungi in Liverwort-Based Biocrust www.ias.is https://doi.org/10.16886/IAS.2019.05 ICEL. AGRIC. SCI. 32 (2019), 43-60 Fungi in liverwort-based biocrust Petra Landmark Gudmundsdottir and Olafur S. Andresson Faculty of Life and Environmental Sciences, University of Iceland, Sturlugata 7, 101 Reykjavík, Iceland. [email protected] and [email protected] ABSTRACT Fungal distribution in a liverwort-based biocrust was examined at different depths (0, 5 and 20 mm) by direct counting using both light and fluorescence microscopy. The DNA-based taxonomic composition of fungi was also determined and differences between depths (above and below 5 mm) were assessed. The fungal biomass was greatest at the surface where large hyphae, sporangia and fungi within plants were more abundant than at 5 mm and 20 mm depth. The texture of the biocrust also differed significantly with depth. Likewise, the analysis of microbial DNA composition revealed a difference between depths, both for the amount of total fungi and of each phylum where the total amount of fungi was highest above 5 mm. Ascomycota fungi were dominant both below 5 mm and near the surface where both their amount and proportion were substantially higher than deeper down. The dark septate Exophiala, Phialocephala and Pseudogymnoascus were the most abundant genera. Keywords: biocrust, biological soil crust, fungal composition, fungal structure, microfungi, Iceland. YFIRLIT Sveppir í hélumosalífskurn Sveppir í íslenskri hélumosalífskurn voru skoðaðir í ljóssmásjá og í flúrsmásjá. Munur á dreifingu sveppa var metinn eftir dýpi (0, 5, 20 mm) og flokkunarfræðileg samsetning hópa í lífskurninni var skoðuð ofan við 5 mm og neðan við 5 mm. Munur var á áferð lífskurnar og útbreiðslu sveppa eftir dýpi. Lífmassi sveppa var meiri við yfirborð þar sem breiðir sveppþræðir, gróhirslur og sveppir á og í plöntum voru í meira magni en á 5 mm og 20 mm dýpi. Samsetningin var jafnframt mismunandi eftir dýpi hvað varðar heildarmagn sveppa og magn einstakra fylkinga. Heildarmagn sveppa var meira í sýnum ofan við 5 mm en neðar. Asksveppir voru ríkjandi í öllum sýnum, bæði ofan við 5 mm og neðan við 5 mm en þeir voru í töluvert meira magni og hærra hlutfalli ofan við 5 mm en neðan. Dökkir sveppir af ættkvíslunum Exophiala, Pialocephala og Pseudogymnoascus voru algengastir. INTRODUCTION arid and dry environments, open woodlands, What is a biological soil crust? unforested grasslands, bare ground, and Biological soil crusts or biocrusts are complex associated with alpine or tundra vegetation. communities in the surface layer of the soil and Even though biocrusts are present in diverse often contain a mixture of various organisms environments they have similarities in function, such as bryophytes, lichens, green algae, fungi, as well as in composition and structure. For cyanobacteria and other bacteria (Belnap et al. example, the structure of biocrusts in hot deserts 2001, Belnap et al. 2016). Biocrusts are found throughout the world, in Australia and North and in many open types of vegetation in various South America, is very similar, but distinctly habitats worldwide such as deserts and other different from biocrusts in cool and cold habitats 44 ICELANDIC AGRICULTURAL SCIENCES such as those found on the Colorado Plateau This stabilizes and protects the soil surface and in the Great Basin of the United States and (Belnap et al. 2001). The soil aggregation in the Arctic (Belnap 2001, Breen et al. 2008, counteracts movement and displacement Williams et al. 2017). by water and wind, decreasing erosion and Climate strongly influences the type maintaining soil moisture. Therefore, biological of biocrust present, especially in tundra soil crusts often act as seedbeds promoting environments (Williams et al. 2016, Rippkin establishment of vascular plants (Elmarsdottir et al. 2018). Availability of moisture affects et al. 2003, Zhang, Aradottir et al. 2016). biocrust abundance as well as composition (Borchhardt et al. 2017). The bryophyte Fungi in biocrust component has higher moisture requirements Biodiversity studies of biological soil crusts than cyanobacteria and lichens. Well-developed have so far focused on cyanobacteria and other biocrusts are generally not found in very dry bacteria as well as bryophytes and lichens that areas. In dry areas biocrusts are usually in early- are components of well-developed biocrusts. successional stages and devoid of organisms There are very few studies on fungi in biocrust with high moisture requirements such as and they remain poorly characterized. These bryophytes. In contrast, biocrusts in areas with few studies are mostly descriptive and little is high precipitation and low temperatures are known about the correlation of fungal diversity often dominated by bryophytes (Bowker et al. with other factors such as nutrient cycling 2016). (Bates, Garcia-Pichel & Nash 2010, Maier et al. Vascular plants are very dependent upon 2016). water availability. Therefore, areas with limited Well-developed biocrusts have greater water availability often have little vascular fungal diversity and abundance than biocrusts vegetation cover. Consequently, there is more in early successional stages. Furthermore, soil surface available for biocrusts in these disturbance has a negative effect on fungal regions. Similarly, short growing seasons and diversity in biocrusts (Bates et al. 2012, Bates, low temperature can impede growth of vascular Nash et al. 2010, Maier et al. 2016). Bacterial plants, favoring lichens, bryophytes and abundance is higher than fungal abundance in biocrusts. Biocrusts have a tendency to occupy biocrust. The bacterial-to-fungal ratio has been bare soils and interspaces between vascular found to be between 1000:1 and 50:1, measured plants. In fact, it has been suggested that with rRNA copy numbers or with biomass biocrusts don’t compete with vascular plants estimations. The distribution and diversity of and some studies have shown that vascular fungi has been found to be patchy, with some plants can benefit from growing on biocrusts areas without hyphae while in others hyphae (Belnap et al. 2001). were abundant (Bates & Garcia-Pichel 2009, Biological soil crusts have different Bates, Nash et al. 2010). successional stages where early successional Microfungi are pronounced in biocrusts and stages are often characterized by low species can be free-living, mycorrhizal or saprophytic richness and domination of cyanobacteria which (Belnap et al. 2001). Although microfungi are contribute both to carbon and nitrogen fixation. believed to be more abundant in biocrust than in The cyanobacterial genus Microcoleus is often soil, this is based on very few studies. The phylum pronounced in early-successional biocrusts, Ascomycota has been shown to be dominant whereas Nostoc and Scytonema spp. are more in biocrust and genera such as Alternaria and likely to be present in late successional stages Acremonium/Phoma are generally present in (Belnap et al. 2001, Belnap et al. 2016). biocrusts (Bates & Garcia-Pichel 2009, Bates, In the top few millimeters of biological soil Nash et al. 2010, Bates et al. 2012, Bates, Nash crust fungal hyphae and cyanobacterial filaments et al. 2010, Maier et al. 2016). form a matrix that binds soil particles together. Members of all the classical fungal phyla FUNGI IN LIVERWORT BIOCRUST 45 have been found in biological soil crusts. Most identified in biocrust from the Colorado Plateau studies have found Ascomycota, Basidiomycota and other regions. E. crusticola is a black yeast, and Zygomycota (Bates, Garcia-Pichel & tolerant of extreme conditions such as shortage Nash 2010, Bates et al. 2012, Bates, Nash et of nutrients and low water availability (Bates et al. 2010, Zhang et al. 2018), but some have al. 2006, Maier et al. 2016). Mortierella, mostly found only two of these phyla (Bates & Garcia- Mortierella alpina, is often found in biocrusts Pichel 2009). Chytridiomycota have also been and is the most common zygomycete (Bates, found in biocrust (Abed et al 2013, Steven et Garcia-Pichel & Nash 2010, Bates, Nash et al. al. 2015). Ascomycota are the most dominant 2010). and have so far been found to account for over A Chinese study on fungi in biocrust found 80% of biocrust fungi (Abed et al. 2013, Bates the composition to be different from previous & Garcia-Pichel 2009, Bates, Garcia-Pichel & studies in desert areas at the genus level and Nash 2010, Bates et al. 2012, Bates, Nash et al. to vary greatly along successional gradients 2010, Zhang et al. 2018). (Zhang et al., 2018). The genera Humicola, The order Pleosporales, within Ascomycota, Endocarpon and Heteroplacidium were found is very prevalent in biocrusts and may represent to be dominant, whereas Alternaria/Lewia the bulk of dark-septate fungi (dematiaceous and Acremonium/Phoma were not detected. fungi; with darkly pigmented hyphae or spores) Humicola has previously been found in desert (Abed et al. 2013, Bates & Garcia-Pichel 2009, biocrusts (Bates, Garcia-Pichel & Nash 2010). Bates, Garcia-Pichel & Nash 2010, Bates, Although publications show few major Nash et al. 2010, Bates et al. 2012, Steven et differences in biocrust fungal composition, most al. 2015). The cell walls of dark-septate fungi research so far has been done in deserts, mainly are rich in melanin which is thought to confer in the USA (Bates & Garcia-Pichel 2009, Bates tolerance to many stress factors such as solar et al. 2012, Bates, Nash et al. 2010, Steven et radiation and extreme temperatures, enabling al. 2016). There have been very limited studies these fungi to survive harsh conditions (Maier on fungal composition in the arctic regions or et al. 2016). Although the order Pleosporales is other cool habitats (Broady & Weinstein 1998, the most abundant and widespread, two other Zhang, Wang et al 2016). Therefore, the scenario orders, Hypocreales within Ascomycota and described might be limited to these regions or Mortierellales within Zygomycota, have also habitats. In a Norwegian study on biocrust in a been found to be widely distributed (Abed et glacier foreland the most common fungi present al. 2013, Bates & Garcia-Pichel 2009, Bates, in the biocrust were Lecythophora, Penicillum, Garcia-Pichel & Nash 2010).
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