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A Survey of Fungal Community Composition Along a Gradient of Recovery on the Mine Sites in the Carolinas

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A Survey of Fungal Community Composition Along a Gradient of Recovery on the Mine Sites in the Carolinas A Survey of Fungal Community Composition along a Gradient of Recovery on the Mine Sites in the Carolinas Ruolin Miao Under the supervision of Dr. Rytas Vilgalys, Department of Biology, Duke University And Dr. Alejandro Rojas, Department of Entomology and Plant Pathology, University of Arkansas April 22, 2019 _______________________________ Research Supervisor _______________________________ Faculty Reader _______________________________ Director of Undergraduate Studies Honors thesis submitted in partial fulfillment of the requirements for graduation with Distinction in Biology in Trinity College of Duke University Abstract In the era of Anthropocene, an increasing part of the terrestrial environments is losing their ecosystem services and function, negatively affecting both human economics and the ecological system. Phytoremediation, the use of plants to reverse degradation and to restore ecological function, has been a promising approach. However, the symbiotic soil microbiota that influence the effectiveness of this method is not fully understood. I sampled the soil and roots of Pinus spp. (pines) at four sites along a gradient of vegetation recovery on the Superfund Site Brewer Gold Mine (SC), the Henry Knob Mine (SC), and Russell Gold Mine. The acidity, nutrient profile and heavy-metal contamination of collected soil is determined. DNA is extracted from the soil and root samples with PowerSoil DNA Isolation Kit, followed by preparation of multiplex PCR samples of the ITS region. Sequence reads generated through Illumina Miseq is processed through QIIME pipeline and taxonomy assigned through UNITE database. The results show a pattern of succession in fungal communities along a recovery gradient. While the mycorrhizal fungi on the least recovered site are dominated by Rhizopogon sp. and Pisolithus sp., sites with more recovered vegetation reveal a more diverse array of symbiotic fungi, including Amanita sp. and Russula sp.. These diverse fungi, although came later in the succession pattern, likely brings more diverse benefits to help their hosts cope with the stressful environment. This “bioprospecting” method could be applied to extract and amplify symbiotic fungi to facilitate revegetation efforts. Introduction A major feature of the Earth’s most current geological epoch, the Anthropocene, is the unmistakeable impact of human activity on ocean and terrestrial environments. One prime example of major terrestrial impacts are mine sites, whose activities result in loss of topsoil, reduced soil fertility and biodiversity, and high concentrations of pollutants such as toxic metals (Wang, 2017). The use of plants has been proposed as a major mechanism to reverse degradation processes and restore ecological function at mine sites through phytoremediation (Singh, Raghubanshi, & Singh, 2002), which is assisted by mutualistic plant-associated microbes that play an important role in revegetation and succession (Dickie et al., 2013). Mutualistic symbiotic fungi, including mycorrhizal fungi and endophytic fungi, confer a range of fitness benefits that help plants adapt to stress, including improved nutrient acquisition, and tolerance to drought, heat, metals, herbivory, and organic contaminants (Marrs, 2016). [Write about mycorrhizal fungi in particular] The study of such fungi-plant symbiosis on mining-impacted sites could provide valuable insights into the utilization of beneficial fungi to facilitate ecological restoration. A number of studies have demonstrated the potential of symbiotic fungi to assist plant survival at heavy-metal contaminated sites. Mycorrhizal fungi in particular are known to improve the metal tolerance of their host plants. For example, AM fungi have been reported to occur on the roots of Viola calaminaria in Zn/Pb-rich soil and Berkheyla coddii in Ni-rich soil, accumulating and immobilizing heavy metals in their structures (Gaur & Adholeya, 2004). In experiment with zinc-rich soil, ectomycorrhiza Suillus bovinus have been shown to improve the nutrient uptake and growth of Pinus sylvestris (Adriaensen, Vangronsveld, & Colpaert, 2006). Similar benefits to hosts have been observed in endophytic fungi: Shi et al. show that Fusarium sp. and Penicillium sp. associated with Brassica napus improved the rape biomass and metal extraction efficiency of their host in Cd and Pb contaminated soil (Shi et al., 2017). Many of these in-vitro studies have focused on a limited array of fungi. The most heavily studied fungal genera include Suillus (Adriaensen, van der Lelie, Van Laere, Vangronsveld, & Colpaert, 2003; Colpaert, Vandenkoornhuyse, Adriaensen, & Vangronsveld, 2000), Thelephora (Van Tichelen, Colpaert, & Vangronsveld, 2001), and Glomus (Amna et al., 2015). Indigenous fungal communities likely hold other promising fungal strains for phytoremediation that may adapt better to the local environment, establish a more mutualistic interaction with their host and pose less interruption to the surrounding soil microbiota (Faye et al., 2013; Mummey, Antunes, & Rillig, 2009). Study of these fungal communities could provide new insights into the co-existence of multiple strains of symbiotic fungi under various ecological stresses (different heavy-metal contamination, acidity, drought). Early-stage, or early successional fungi are known to inhabit mineral soils of a low nutrient content or with extreme pH values (Münzenberger, Golldack, Ullrich, Schmincke, & Hüttl, 2004). Environmental filtering acts on the fungal communities on mine sites: ECM communities are influenced strongly by the soil features of the sites, such as the low levels of organic matter, soil structure, pH values, soil temperature and moisture (Huang et al., 2012; Staudenrausch, Kaldorf, Renker, Luis, & Buscot, 2005). ECM fungal species that are found on the roots of Pinus massoniana growing on Pb-Zn mine sites includes Cenococcum geophilum, Rhizopogon buenoi, Tomentella ellisii, Inocybe curvipes and Suillus granulatus on Pinus massoniana (Huang et al., 2012). Pisolithus tinctorius is a typical, widespread early-stage ECM fungus, reported to be well- adapted to the low pH and high temperatures of anthracite and hard coal spoils (Schramm, 1966; Marx, 1975). Fungal community might shift through the succession. The fungal communities in pioneer pine forests on metal mines in Belgium revealed that it is initially dominated by dark Ascomycota, but metal tolerance basidiomycetes such as Suillus luteus become more frequent within two years (Op De Beeck et al., 2015). A review of studies on ectomycorrhizal fungal genera across soil chronosequences suggests putative trait groupings of different genera: early successional genera likely include ones with low host-specificity, forming small, inconspicuous sporocarps that are long-term persistent (Cenococcum, Tomentella / Thelephora, Inocybe, Cortinarius and Laccaria); early-mid successional genera may include ones with high host- specificity and large sporocarp (Rhizopogon and Suillus); and the genera most common in mature ecosystems include Amanita, Russula, Lactarius and Boletus (Dickie et al., 2013). In reforestation of the mine sites, inoculation of selected ECM fungi potentially confers key advantages for tree seedlings to adapt to environmental stress and adverse substrates during the first few years after outplanting (Kałucka & Jagodziński, 2016). Such inoculation is most effective when fungal inocula are adapted to the environmental conditions of transplantation sites (Rincón, de Felipe, & Fernández-Pascual, 2017). A better understanding of the ECM fungal community indigenous to the mine sites and surrounding forest areas is therefore crucial to facilitate better restoration of sites impacted by anthropogenic activities. In this study, the fungal communities associated with pines (Pinus spp.) were studied on three abandoned mineral and metal mine sites in the Carolinas—the Brewer Gold Mine, Henry’s Knob Mine (kyanite), and Russell Gold Mine. The goals of this study were to characterize the fungal community, in particular the ECM fungi, on pines growing on the mine sites and to evaluate the effects of soil characteristics on these communities. Methods Field sites Brewer Gold Mine Brewer Gold Mine (BGM) is a Superfund site near Jefferson, South Carolina. BGM has mined significant ore from several open pits (over 12 million tons of ore and waste rock from 1987 to 1995). When EPA took over the site in 1995, serious concerns were raised over multiple contamination sources, including pollution from the cyanide solution used for extracting gold, acid mine drainage (AMD) and heavy-metal contamination. BGM thus serves as a prime field site to study plant-fungal symbiosis under multiple stress factors. Upon consultation with our mine site contact, we decided on four experimental sites (Figure 1) with one control site in the nearby forest. From each site, we collected three soil samples under Pinus taeda (loblolly pine) and the corresponding root samples. Henry’s Knob Mine The Henry’s Knob Mine (HKM) was utilized for the extraction of kyanite, an aluminum silicon oxide used in the manufacture of high-alumina brick and other high temperature, refractory materials. Mining activities ceased in the 1970’s and with common duty of care at that time, mine tailings were present at several large areas of fine grained mineral sediment located down slope of former mineral processing facilities. The site is approximately 185 acres in size, mainly a combination of wooded tree growth and revegetated tailings impoundments. We collected
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