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The Diversity of Microfungi in Peatlands Originated from the White Sea

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The Diversity of Microfungi in Peatlands Originated from the White Sea Mycologia, 108(2), 2016, pp. 233–254. DOI: 10.3852/14-346 # 2016 by The Mycological Society of America, Lawrence, KS 66044-8897 Issued 19 April 2016 The diversity of microfungi in peatlands originated from the White Sea Olga A. Grum-Grzhimaylo1 cycle by virtue of their significant peat deposits White Sea Biological Station, Faculty of Biology, that contain 45–50% carbon (Thormann 2006b). – Lomonosov Moscow State University, 1 12 Leninskie Gory, The importance of peatlands for the global C cycle is 119234, Moscow, Russia, and Faculty of Biology, – illustrated by the fact that northern peatlands store St Petersburg State University, 7 9, Universitetskaya nab., – 5 6 9 199034, St Petersburg, Russia 180 277 Gt C (1 Gt 1 10 metric tons), which con- stitutes approximately 10–16% of the total global terres- Alfons J.M. Debets trial detrital C (Thormann et al. 2001a). Laboratory of Genetics, Plant Sciences Group, Wageningen Bogs are a dominant peatland type in the north of University, Droevendaalsesteeg 1, 6708PB, Wageningen, the Netherlands Russia. Coupled with spruce forest, raised bogs prevail in the taiga zone in northeastern Europe. Coastal raised Elena N. Bilanenko bogs predominate along the White Sea coast (Schulze Department of Mycology and Phycology, Faculty of Biology, et al. 2002, Yurkovskaya, 2004). Raised bogs and aapa Lomonosov Moscow State University, 1-12 Leninskie Gory, fens (also called aapa mires) are the zonal mire com- 119234, Moscow, Russia plex types of boreal regions (Laitinen et al. 2005). Raised bogs are ombrotrophic ecosystems that receive water and nutrients solely from atmospheric precipita- Abstract: The diversity of culturable filamentous tion. They are commonly dominated by species of microfungi in peat and sediments of four peatlands Sphagnum mosses, Picea mariana and members of the at the coastal zone of Kandalaksha Bay of the White Sea (Murmansk region, Russia) was studied by culture Ericaceae, including species of Rhododendron spp., Andro- methods on standard and selective media. Annually meda spp. and Vaccinium spp. (Thormann et al. 1999, 100 samples were collected from the bogs 2007–2010. Thormann 2006a). Aapa fens are more minerotrophic Based on morphological, molecular markers and cul- (i.e. they receive their nutrients both from precipita- tural features, 211 taxa were identified. Fungal com- tion and the surrounding land because of their hydro- munities observed at the peatlands were influenced logical regime). These peatlands consist of a lake, mostly by their sea origin. We discovered a large differ- elongated Sphagnum-formed hummocks and water ence between fungal communities from the peat and channels (Keränen and Kalpio 2001; Laitinen et al. the sediments of the peatlands. In contrast to the sedi- 2005, 2007). Aapa mire is a Finnish term for a large, ments, the fungal community of the peat was found to complex, cold-climate wetland. This is a mire-system be consistent throughout sampling sites. Fungi with type, the central parts of which are characterized by specific ecophysiology, such as Sphagnum-decomposing minerotrophy and near to mire inherent influence. species (Oidiodendron griseum, O. tenuissimum, Penicil- These systems may receive supplementary nutrition to lium spinulosum, P. thomii, Talaromyces funiculosus), their central parts, in addition to marginal parts and ‐ psychrotolerant and associated with insects species brook sides, through meltwater from the surround (Pseudogymnoascus pannorum, Tolypocladium spp.), typi- ing area. Aapa mires are morphologically variable cal marine species (Acremonium spp.) were found. In (Laitinen et al. 2007). addition, different types of sterile mycelia were charac- The annual accumulation of peat is caused by rela- teristic for the researched peatlands. tively slow organic decomposition by microorganisms because of extremely unfavorable conditions: lack of Key words: fungal diversity, fungi decomposing Sphagnum, fungi in sediments, molecular identifica- oxygen, low temperatures, high acidity and humidity, tion, psychrotolerants the presence of inhibitory complex phenolic compounds from specific vegetation (mostly Sphagnum spp.) and an inherent lack of microbial diversity to degrade the INTRODUCTION most complex polymers of peat (Untiedt and Müller Peatlands cover about 4% of the world, more than 1984, Tsuneda et al. 2001, Thormann et al. 2002, 10% of the territory of Russia and about 70–80% of Rice et al. 2006, Andersen et al. 2010). the White Sea coastal territory (Yurkovskaya 2004). In White Sea coastal raised bogs, peat consists of Peatlands accumulate peat, partially decayed plant the complex of plant material dominated by Sphagnum material, and play a significant role in the global carbon fuscum (Yurkovskaya 2004). Fungi, together with het- erotrophic bacteria, are the main decomposers of Submitted 19 Sep 2014; accepted for publication 20 Oct 2015. the organic matter in peat (Pankratov et al. 2005; 1 Corresponding author. E-mail: [email protected] Gilbert and Mitchell 2006; Thormann et al. 2001a, b, 233 234 MYCOLOGIA FIG. 1. Map of the Kindo Peninsula with four studied peatlands tagged: A 5 Verkhnee Peatland, B 5 Krugloe Peatland, C 5 Ershovskoe Peatland, C(1) 5 Ershovskoe Verkhnee Lake, C(2) 5 Ershovskoe Nizhnee Lake, D 5 Kislosladkoe Peatland, WSBS 5 White Sea Biological Station. 2006a, b, 2007; Andersen et al. 2010). In the northern four peatlands at different altitudes above sea level peatlands fungal diversity estimates are 22–55 species (1.5–87 m) representing different stages of bog forma- per peatland. Those species have a capacity for living tion. Fungi were identified with morphological and and physiological activity in peat (Nilsson and Rülcker cultural features as well as DNA sequence data (ITS 1992, Czeczuga 1993, Thormann et al. 2001b). rDNA region, along with SSU and LSU rDNA). We The respective role of fungi in litter decomposition characterized the composition, abundance and spatial and the multiple-factor peat-forming process in peat- distribution of species in fungal communities from lands is still poorly studied. Most peatlands are in the peatlands in connection with the age of the reservoirs northern hemisphere (Thormann et al. 2007), how- and their contact with the sea. ever, little is known about fungal biodiversity of the northern peatlands. Some data is available of peatland MATERIALS AND METHODS fungi from western Siberian and central Russia Study area.—It is near the Karelian coast of Kandalaksha Bay (Golovchenko et al. 2002, Kachalkin et al. 2005, of the White Sea (FIG. 1) near the WSBS (66u349N, 33u089E). Grum-Grzhimaylo and Bilanenko 2009, Filippova and Kindo Peninsula, where the station is located, is near the Arc- Thormann 2014) but almost no data is available for tic Circle. The geographic position of lakes determines the the fungi from the peatlands in northwestern Russia. climatic conditions under which their hydrological regime The peatlands at the Kandalaksha Bay of the White is formed. In this case this is a long winter with an average Sea have a unique origin. They appear as a result of a daily temperature of −11 C in Jan and a relatively short part of the sea becoming isolated during rapid land humid summer with a maximum precipitation in Aug and a uplift (0.5 cm/y), followed by both demineralization mean temperature of 14 C in Jul (Shaporenko et al. 2005). Annual precipitation is 300–400 mm (Bubnova 2005). Geo- and the development of bogs (Shaporenko et al. 2005, morphologically the region lies on the northern margin of Pantyulin and Krasnova 2011). In this process the Pribelomorskaya Lowland. The maximum elevation of the succession of marine biota by freshwater takes place, area is less than 100 m. which is common for peatlands. Fungi, functioning as decomposers, symbionts, parasites and pathogens, Description of the investigated peatlands.—Four investigated are associated with the evolution of the reservoirs that peatlands are located, ranging from the lowest to the highest have a sea origin (their number is evaluated from one point of the peninsula and represent almost all evolution to several hundred at Kandalaksha Bay), but the data stages of bogs in this area of the White Sea coast (FIG.1,TABLE on mycobiota of these systems are hardly discussed in I). Two of them represent raised bog-type peatlands (Verkh- the literature. nee, Krugloe; FIGS. 2A, 2B), the third is a transition aapa fen (Ershovskoe; FIG. 2C) and the fourth is a brackish lake detach- The aim of our research was to investigate fungal ‐ ing from the sea (Kislosladkoe; FIG. 2D). Kislosladkoe Lake diversity in the peatlands around the White Sea Biolog has both marine and continental features. There is a combi- ical Station (WSBS) of Lomonosov Moscow State Uni- nation of typical littoral vegetation with bog plants depending versity in northwestern Russia. The fungi were isolated of coast parts in this peatland. The characteristics of aapa fen from the peat and sediment samples taken from types were described in detail by Laitinen et al. (2007). TABLE I. Description of the investigated peatlands Water Age Max level in Peatland (year) Alti- Peat depth of sampling Dominant vegetation Latitude/ (Shilova tude Type of depth sampling pH of places longitude (in No. Name 2011) (m) peatland (m) (m) samples (cm) Trees Shrubs/subshrubs Herbs Mosses/lichens centers of lakes) 1 Verkhnee 8400¡110 87 Raised bog 4.6 2.0 Peat 4.1, −20 Pinus Chamaedaphne Drosera rotundifolia, D. Pleurozium schreberi, 66u32937.0206″/ sediments sylvestris, calyculata, anglica, Eriophorum Sphagnum fuscum, 33u5950.4348″ 6.0 Betula Calluna latifolium, Sph. capillifolium, nana vulgaris, Menyanthes trifoliata Sph. papillosum, Rubus Sph. magellanicum, G RUM chamaemorus, Sph. majus, Oxycoccus Cladonia -G microcarpus, rangiferina, Cl. RZHIMAYLO Ledum palustre alpestris, Cl. mitis, Cetraria islandica, Nephroma sp. 2 Krugloe 3970¡40 27.5 Oligotrophic 2.4 1.4 Peat 4.1, −10 Pinus Calluna vulgaris, Drosera rotundifolia, D. Pleurozium schreberi, 66u32932.8416″/ aapa sediments sylvestris, Rubus anglica, Baeothryon Sphagnum 33u8922.4592″ ET AL 6.0–6.5 Betula chamaemorus, caespitosum papillosum, Sph.
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