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Fungal Communities in Ancient Peatlands Developed from Different Periods in the Sanjiang Plain, China

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Fungal Communities in Ancient Peatlands Developed from Different Periods in the Sanjiang Plain, China RESEARCH ARTICLE Fungal communities in ancient peatlands developed from different periods in the Sanjiang Plain, China Zhenqing Zhang1,2☯, Xue Zhou1☯, Lei Tian1,3, Lina Ma1, Shasha Luo1, Jianfeng Zhang1, Xiujun Li1, Chunjie Tian1* 1 Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, China, 2 Key Laboratory of Wetland Ecology and Environment, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, China, 3 University of a1111111111 the Chinese Academy of Sciences, Beijing, China a1111111111 a1111111111 ☯ These authors contributed equally to this work. a1111111111 * [email protected] a1111111111 Abstract Peatlands in the Sanjiang Plain could be more vulnerable to global warming because they OPEN ACCESS are located at the southernmost boundary of northern peatlands. Unlike bacteria, fungi are Citation: Zhang Z, Zhou X, Tian L, Ma L, Luo S, often overlooked, even though they play important roles in substance circulation in the peat- Zhang J, et al. (2017) Fungal communities in land ecosystems. Accordingly, it is imperative that we deepen our understanding of fungal ancient peatlands developed from different periods in the Sanjiang Plain, China. PLoS ONE 12(12): community structure and diversity in the peatlands. In this study, high-throughput Illumina e0187575. https://doi.org/10.1371/journal. sequencing was used to study the fungal communities in three fens in the Sanjiang Plain, pone.0187575 located at the southern edge of northern peatlands. Peat soil was collected from the three Editor: Erika Kothe, Friedrich Schiller University, fens which developed during different periods. A total of 463,198 fungal ITS sequences GERMANY were obtained, and these sequences were classified into at least six phyla, 21 classes, Received: May 15, 2017 more than 60 orders and over 200 genera. The fungal community structures were distinct in Accepted: October 23, 2017 the three sites and were dominated by Ascomycota and Basidiomycota. However, there were no significant differences between these three fens in any α-diversity index (p > 0.05). Published: December 13, 2017 Soil age and the carbon (C) accumulation rate, as well as total carbon (TC), total nitrogen Copyright: © 2017 Zhang et al. This is an open (TN), C/N ratio, and bulk density were found to be closely related to the abundance of sev- access article distributed under the terms of the Creative Commons Attribution License, which eral dominant fungal taxa. We captured a rich fungal community and confirmed that the permits unrestricted use, distribution, and dominant taxa were those which were frequently detected in other northern peatlands. Soil reproduction in any medium, provided the original age and the C accumulation rate were found to play important roles in shaping the fungal author and source are credited. community structure. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This work was financially supported by the Science Foundation of Chinese Academy of Sciences (XDB15030103), the National Basic Introduction Foundation (2016YFC0501202), Key Laboratory Peatlands, worldwide and particularly in the northern (boreal and subarctic) part, are shown Foundation of Mollisols Agroecology (2016ZKHT- 05), the Key Technology Research and to be important participant in global C cycle in the recent past [1]. Despite covering only 6±8% Development Program of CAS during the ª13th of the terrestrial ecosystems, northern peatlands store 550Pg C [2], accounting for 25±33% of Five-Year Planº (Y6H2043001), the National the world's soil C [3]. The rate of C accumulation is controlled more by changes in annual PLOS ONE | https://doi.org/10.1371/journal.pone.0187575 December 13, 2017 1 / 16 Fungal communities in ancient peatlands Natural Science Foundation of China (41671094, plant productivity than by decomposition [4]. In particular, the reason for peatlands function- 41571255, 31370144), and the Natural Science ing as a C sink is that more C is fixed by its vegetation than it is lost through the outflow of dis- Foundation of Jilin Province (20140101017JC). solved organic C and emissions of CO2 and CH4 [5, 6]. However, there is a growing concern Competing interests: The authors have declared that the ongoing and future global warming will change the C cycling in these ecosystems, that no competing interests exist. making peatlands return the previously captured C to the atmosphere via releasing CO2 and/ or CH4, which would possibly accelerate the pace of global warming [7±10]. Many studies have shown that fungi play a crucial role in the soil ecosystem [11±13]. For example, mycorrhizal fungi contribute to the growth of plants by providing root-available nitrogen and phosphorus [14]. During the initial stage of plant litter decay, saprophagous fungi are more important than bacteria in the degradation of fresh litter into less labile organic matter [15]. The fungal communities, activities, and effects in the peatlands of America, Europe, and Canada have been studied well. Lin et al. [16] found that dominant fungal taxa at bog and fen sites in the peatlands of northwestern Minnesota were Ascomycota, Basidiomy- cota, and Zygomycota, and the ammonia, dissolved organic carbon (DOC), and dissolved organic nitrogen (DON) concentrations were more important than pH in structuring fungal community structure. The same dominant fungal taxa were detected in the ombrotrophic peatlands of northern England by Liu et al. [17]. They determined that fungal community composition was significantly affected by organic matter (OM), moisture, phosphorus, and ammonium. Sun et al. [18] reported that Ascomycota and Basidiomycota were the majority groups in the boreal peatlands in Finland, and the dominant tree species and the availability of certain nutrients (Ca, P, and Fe) had a strong effect on the composition of fungal communities. Myers et al. [19] stated that fungal activity became increasingly important and was negatively correlated with pH and total peat Mg concentrations in ombrotrophic peatlands located in southern Canada. Soil age and the C accumulation rate were reportedly to be important factors of fungal community structure in other ecosystems. Several studies found that fungal commu- nities shifted significantly across chronosequences in a forest ecosystem [20±22]. Zhang et al. [23] found that C accumulation promoted macroaggregates formation and reduced the effec- tive diffusion coefficient of oxygen; thus, they identified changes in microhabitats and a shift in microbial community when they investigated the linkage between organic C accumulation and microbial community dynamics in a sandy loam soil. However, there are few studies on the fungal community in the Sanjiang Plain, leading to the lack of a high-quality curated database for taxonomic assignment. The Sanjiang Plain, located in the temperate climate region, is the largest area of freshwater marshlands in China [24]. These peatlands could be more vulnerable to global warming because they are primarily located at the southern boundary of northern peatlands [1]. Thus, it is imperative that we deepen our understanding of the microorganisms, particularly fungi, in this ecosystem. In this study, high-throughput Illumina sequencing of ITS rRNA genes was used to study the fungal communities in the Sanjiang Plain at the southern edge of northern peatlands. Peat soils were collected from three fens which began development at different time periods. The greater sequencing detail achieved by the high-throughput sequencing allowed the capture of the less abundant and uncultured taxa, thus enabing a more thorough characterization of peatland fungal diversity. The chronological sampling approach further facilitated the analysis of poten- tial linkages of fungal communities with soil age as well as the C accumulation rate. Materials and methods Study area and sampling description Peat cores were sampled from three different minerotrophic fens Shenjiadian (S), Honghe (H), and Qindelie (Q) in the Sanjiang Plain (129Ê110-135Ê050 E, 43Ê490-48Ê270 N), China PLOS ONE | https://doi.org/10.1371/journal.pone.0187575 December 13, 2017 2 / 16 Fungal communities in ancient peatlands Fig 1. Map of the study region showing locations of the sampling sites in the Sanjiang Plain, which was generated using ArcGIS 10.0 (http://www.esrichina.com.cn/). https://doi.org/10.1371/journal.pone.0187575.g001 (Fig 1). No specific permits were required for our field studies and our work did not involve endangered or protected species. The three fens started to develop during different time peri- ods during the Holocene [25]. Over 70% of this region is dominated by fresh water wetlands developing in ancient riverbeds and waterlogged depressions, and approximately 30% (or nearly 3.3 × 104 ha) of this region is covered by peatlands, which developed under certain topo- graphic conditions during or before the Holocene [26]. The study area has a temperate humid to sub-humid continental monsoon climate. The mean annual temperature ranges from 1.4ÊC to 4.3ÊC, with an average maximum of 22ÊC in July and an average minimum of -18ÊC in Jan- uary. The mean annual precipitation is 500±650 mm, and 80% of rainfall occurs between May and September [27]. The sampled fens receive water inputs from groundwater as well as PLOS ONE | https://doi.org/10.1371/journal.pone.0187575 December 13, 2017 3 / 16 Fungal communities in ancient peatlands
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