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Chytrid Fungi Associated with Pollen Decomposition in Crater Lake, Oregon Kathleen A

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Chytrid Fungi Associated with Pollen Decomposition in Crater Lake, Oregon Kathleen A APPLIED & ENVIRONMENTAL MICROBIOLOGY • 83 CHYTRID FUNGI ASSOCIATED WITH POLLEN DECOMPOSITION IN CRATER LAKE, OREGON KATHLEEN A. PAGE* AND MEGHAN K. FLANNERY DEPARTMENT OF BIOLOGY, SOUTHERN OREGON UNIVERSITY, ASHLAND, OR USA MANUSCRIPT RECEIVED 25 OCTOBER 2017; ACCEPTED 27 JANUARY 2018 Copyright 2018, Fine Focus. All Rights Reserved. 84 • FINE FOCUS, VOL. 4(1) ABSTRACT We identified chytrid fungi that were attached to pine pollen on the surface of Crater Lake. Fungi were identified by large subunit (LSU) rRNA gene sequencing of lake pollen extracts and by isolation of a chytrid fungus that was present on the pollen. LSU rRNA PCR products were cloned, sequenced and identified. The majority of eukaryotic LSU rRNA sequences associated with pollen were found to be members of the chytrid order Rhizophyidiales. A fungal CORRESPONDING isolate was characterized culturally, morphologically, and AUTHOR by DNA sequencing and was identified as a member of the genus Paranamyces, in the order Rhizophydiales. In addition, Kathleen A. Page protist LSU rRNA sequences from the phylum Ciliophora [email protected] were found. The concentrations of dissolved organic matter, nitrogen, and phosphate in surface water that had visible KEYWORDS pollen rafts increased according to the concentration of pollen in the water. Each of these nutrients was detected • Chytrid at several fold higher levels in water with pollen rafts as • Pollen compared to surface water lacking pollen rafts. These results • Crater Lake ecosystem • Food Webs provide evidence for the role of chytrid fungi in nutrient • Fungal Aquatic Ecology release from pollen deposited on Crater Lake. INTRODUCTION The occurrence of pollen in Crater Lake: depth of 594 m. It is a nitrogen limited, seasonal pine pollen deposition is a source oligotrophic lake that supports a relatively of allochthonous organic matter for Crater low density of phytoplankton, heterotrophic Lake, Oregon. Crater Lake is a high-elevation, bacteria, fungi, zooplankton, and fish (12). collapsed volcanic caldera lake and the During spring and early summer, coniferous deepest lake in the United States. It has an forests in the vicinity of Crater Lake produce average depth of 350 m and a maximum massive amounts of wind-dispersed pollen, APPLIED & ENVIRONMENTAL MICROBIOLOGY • 85 primarily from pine trees including Pinus production and zooplankton biomass in contora and Pinus ponderorsa (35). Pine oligotrophic lakes (16). Chytrid fungi are pollen grains have air bladders that allow often observed attached to pollen grains that them to float on water and form yellow float on lake surfaces. Unlike most aquatic aggregates known as pollen rafts. The microbes, chytrids have the ability to break appearance of pollen rafts on Crater Lake down the outer exine wall of pollen to and on many Northern forest lakes is a obtain nutrients (22, 38, 41). Chytrids that yearly occurrence (7, 16, 33, 44). Terrestrial grow on pollen grains can complete their organic matter does not flow readily into life cycle attached to pollen (15) and are Crater Lake; it is fed by rain, snowmelt, and considered to be major pollen decomposers groundwater. Other than a few small springs along with bacteria (33). Once the exine wall on the steep caldera walls, there are no stream is breached, a variety of other organisms can inputs and sources of allochthonous organic participate in pollen decomposition. Organic matter are presumed to be scarce. Crater matter released from pollen serves as a Lake has seasonal stratification of the water growth substrate for heterotrophic organisms. column and deep-water mixing events every Mineralized phosphate and nitrogen from 2 to 5 years. Pollen dispersal occurs during organic matter decomposition supports summer stratification when warmer water the growth of phytoplankton (4). The size floats on top of colder, denser water. This of pollen grains and their buoyancy make effect provides stability within the photic them susceptible to zooplankton grazing. zone and would be expected to favor growth Partial microbial digestion of pollen greatly of microbial communities associated with increases the nutrient quality of pollen for buoyant pollen. However, pollen grains are zooplankton because zooplankton lack the highly refractory nutrient sources. When ability to break down the outer pollen wall not colonized by microorganisms, they (32). In addition, chytrid zoospores are eventually sink and can be preserved intact consumed by zooplankton and have been in sediments for millennia (34). Because shown to promote their growth (22). Thus, pollen had not yet been studied as a nutrient pollen infection by chytrid fungi initiates source in Crater Lake, we set out to discover food webs that nourish primary producers, if the pollen is subject to frequent microbial heterotrophic microbes and larger consumers colonization and what role, if any, fungi play such as zooplankton. The role of chytrid in its decomposition. fungi in lentic food webs has received little attention, perhaps because of its seasonal Release of nutrients from pollen in support of pollen dependence and difficulty in fungal aquatic food webs: pollen is rich in fatty acids identification (20). Because of the crucial and supplies organic and mineral nutrients role that chytrid fungi play in nutrient when broken down by microorganisms release from pollen, we sought to identify (28, 32). Conifer pollen inputs have been and culture pollen-associated chytrids from shown to increase nutrient levels, primary Crater Lake and compare dissolved nutrient 86 • FINE FOCUS, VOL. 4(1) levels in pollen rafts relative to lake water phylum of fungi that reproduces with lacking pollen. flagellated spores known as zoospores. These organisms, commonly called chytrids or Aquatic food webs were initially imagined zoosporotic fungi, are genetically diverse and as linear food chains from phytoplankton- have been shown to occupy a basal position produced organic matter to zooplankton in fungal phylogeny (10). There are five and animals such as fish. The current taxonomic orders within Chytridiomycota, view is more complex and includes the with Rhizophydiales having the majority of consideration of allochthonous nutrients described genera and species (30). Two other and the roles of heterotrophic bacteria and newly recognized phyla, Blastocladiomycota fungi (36, 37). Heterotrophic microbes thrive and Neocallimastigomycota, are similarly in most aquatic environments, including comprised of zoosporotic fungi although Crater Lake, and participate in food webs these phyla have relatively few species and microbial loops (9, 43). Most of the represented within them (19). The available organic matter in aquatic systems morphologically distinct features of chytrids is not readily digestible by organisms other are their sporangia and their flagellated than heterotrophic bacteria and fungi (6, 8). zoospores, which are produced within the Heterotrophic microbes effectively consume sporangia. In the case of eucarpic sporangia, organic matter and serve as food sources filamentous rhizoids are produced, which for larger microbes and zooplankton. In are attached to the sporangia. Zoospores addition, they are able to mineralize and develop into germlings, which are the release phosphate and nitrate that are often precursors of sporangia. Zoospores and/ limiting nutrients in aquatic ecosystems (9). or germlings typically attach to a nutritive Phytoplankton and heterotrophic microbes substrate such as pollen or phytoplankton and may be in competition for inorganic develop either as epibionts or as endobionts. nutrients, but on the whole, heterotrophs are These morphologic and life cycle features considered to be essential for production of are used to classify zoosporotic fungi (2, 41). mineral nutrients that support phytoplankton In addition, genetic sequences, particularly (4, 38). Until now, pollen has not been large subunit ribosomal RNA sequences, considered as an allonchthonous nutrient in are a valuable aid to identification (2, 42). Crater Lake. Pollen decomposition by chytrid Chytrids are found in aquatic and terrestrial fungi in Crater Lake would support food environments and are often parasites of webs by releasing the nutrients present in phytoplankton or saprophytes with the ability pollen and by promoting chytrid zoospore to break down refractory nutrient sources production. Chytrid sporangia and zoospores such as pollen, chitin, and cellulose (2, 18, serve as food for larger organisms including 20). Lake pollen is considered to be a prime zooplankton and invertebrates (22, 23, 33). nutrient for many aquatic chytrids (15, 33). We hypothesize that Crater Lake pollen is Characteristics of chytrid fungi and their subject to colonization and decomposition growth on pollen: Chytridiomycota is a APPLIED & ENVIRONMENTAL MICROBIOLOGY • 87 by chytrid fungi, and that this leads to an by a general increase in nutrients given that increase in nutrient availability. Food webs Crater Lake is a nutrient-limited ecosystem. at several trophic levels would be supported MATERIALS AND METHODS Sample collection and processing: A Crater sample was processed by pre-filtration Lake research and sample collection permit through a 100-micron filter (to prevent number CRLA-2016-SCI-0005 was obtained clogging) and subsequent filtration through from the National Park Service. Surface a 0.2 micron pore size filter to separate water from Crater Lake was collected in particulates from dissolved nutrients. The 0.5 liter bottles from
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