Distribution and Diversity of Planktonic Fungi in the West Pacific Warm Pool

Distribution and Diversity of Planktonic Fungi in the West Pacific Warm Pool Xin Wang1, Purnima Singh2, Zheng Gao3, Xiaobo Zhang4, Zackary I. Johnson5, Guangyi Wang1,2,6* 1 Department of Microbiology, University of Hawaii at Manoa, Honolulu, Hawaii, United States of America, 2 Collaborative Innovation Center of Deep Sea Biology, Tianjin University Center for Marine Environmental Ecology, School of Environment & Engineering, Tianjin University, Tianjin, China, 3 State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Tai’an, China, 4 Collaborative Innovation Center of Deep Sea Biology, College of Life Sciences, Zhejiang University, Hangzhou, China, 5 Marine Laboratory, Nicholas School of the Environment, Duke University, Durham, North Carolina, United States of America, 6 College of Engineering, California Baptist University, Riverside, California, United States of America Abstract Fungi contribute substantially to biogeochemical cycles of terrestrial and marine habitats by decomposing matter and recycling nutrients. Yet, the diversity of their planktonic forms in the open ocean is poorly described. In this study, culture- independent and molecular approaches were applied to investigate fungal diversity and abundance derived from samples collected from a broad swath of the Pacific Warm Pool across major environmental gradients Our results revealed that planktonic fungi were molecularly diverse and their diversity patterns were related to major phytoplankton taxa and various nutrients including nitrate, nitrite, orthophosphate and silicic acid. Over 400 fungal phylotypes were recovered across this region and nearly half of them grouped into two major fungal lineages of Ascomycota and Basidiomycota, whose abundance varied among stations. These results suggest that planktonic fungi are a diverse and integral component of the marine microbial community and should be included in future marine microbial ecosystem models. Citation: Wang X, Singh P, Gao Z, Zhang X, Johnson ZI, et al. (2014) Distribution and Diversity of Planktonic Fungi in the West Pacific Warm Pool. PLoS ONE 9(7): e101523. doi:10.1371/journal.pone.0101523 Editor: Rodolfo Paranhos, Instituto de Biologia, Brazil Received January 27, 2014; Accepted June 8, 2014; Published July 3, 2014 Copyright: ß 2014 Wang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was partially funded by National Oceanic and Atmospheric Administration (NOAA) grants NA04OAR4600196 (GWY) and NA09AOR4170060 (GWY, by the US Department of Energy award (DE-FG36-08GO18180) (GWY), by NSF Grant OCE05-26462 (ZJ) and OCE05-50798 (ZJ), and funded by National Science Foundation of China grant 31170109 (GYW) and Shenzhen Development and Reform Commission grant 835 (GYW). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * Email: [email protected] Introduction coastal upwelling ecosystem off central Chile [17] and the Hawaiian coastal waters [13]. These filaments or aggregates can The ‘microbial loop’ hypothesis depicts microbes as a central reach up to 20 mm in diameter and over 50 mm long and are player of marine matter and energy fluxes [1]. Molecular comparable to fungal mycelia detected in deep-sea sediments [18] taxonomy and ecological genomics have revealed the efficiency and water-stable aggregates associated with mycorrhizal fungi in with which organic carbon is processed by marine microbes in the soils [19]. In seawater, organic aggregates represent a major surface waters of the ocean [2]. Specifically, heterotrophic bacteria growth habitat for planktonic microbial communities. The and archaea are found to be largely involved in carbon and combined metabolic activities of fungi and prokaryotic microbes nutrient cycling in both coastal and oceanic waters [2,3]. Although can promote a highly efficient conversion of particulate organic heterotrophic eukaryotic microbes are well documented in the matter (POM) to dissolved organic matter (DOM) in seawater ocean, their diversity and function remain relatively unknown. [17,20]. Furthermore, fungal biomass and diversity display spatial Particularly, large populations of planktonic fungi (i.e., filamentous and temporal variations in the coastal marine ecosystems [5,17]. free-living fungi and yeasts, and those associated with planktonic During the summer, fungal biomass can reach up to ,6 mg C/L particles or phytoplankton) have long been known to exist in of surface seawater [17] and the high fungal biomass was reported coastal and oceanic waters [4,5], but their diversity and ecological to be comparable to that of bacterioplankton in the coastal water function are still one of the most under-studied microbial topics. [21]. The vertical profile of fungal biomass and diversity Fungi are key components of the biosphere, performing a wide concurred with those of primary productivity and/or physical range of biogeochemical and ecological functions across disparate parameters of the water columns (e.g., temperature and oxygen) environments [6,7], and are particularly well-known for their [5,17]. Clearly, planktonic fungi are an important microbial important role in processing detrital organic matters from plants component in the coastal marine ecosystems and, like other [8]. Marine yeasts have long been known to be ubiquitous in heterotrophic microplankton, are active in the water column and seawater [9–11]. A typical milliliter of seawater contains several responding to primary production activity and organic matter thousands of fungal cells (or propagules) [12]. In freshwater availability [13,17,21]. ecosystems, fungal biomass can account for as much as 18–23% of In our previous study, we observed a novel diversity of the total mass of detritus [14–16]. Recently, fungal mycelia were planktonic fungi and their interesting relationship with biological found to be present as individual filaments or aggregates in the and physical features of seawater in the Hawaiian coastal waters PLOS ONE | www.plosone.org 1 July 2014 | Volume 9 | Issue 7 | e101523 Diversity of Marine Mycoplankton [5]. In this study, we focused on the diversity and ecology of mycoplanktonic communities in oceanic waters with the intention to gain insight into the following questions. What is the fungal diversity in the West Pacific Warm Pool? How is the fungal diversity and abundance partitioned in this oceanic ecosystem? Is a certain phylum of fungi dominant at a given location? How does the fungal diversity correlate with bacterioplankton and primary producers? Results and Discussion Fungal diversity and major phyla abundance in the open ocean To assess the abundance and diversity of planktonic fungi in the open ocean, we collected seawater samples from five depths in the euphotic zone from stations across an open ocean transect from the Hawaiian coast to Australia (Figure S1 in File S1). A total of 959 clones were selected from 30 clone libraries of the internal transcribed region (ITS) region of the ribosomal RNA genes for sequencing analysis. Sequence analyses identified 411 distinct phylotypes (99% similarity) from 6 different stations (Tables S1 and S2 in File S1). Such a high diversity of planktonic fungi (and/ or fungi like eukaryotes) was reported for the first time from the oceanic waters. Fungal diversity found in this study was much higher than that of previous report in Hawaiian coastal waters [5]. The diversity discrepancy clearly ascribed to differences in diversity analysis methods (clone library vs. DGGE), and primers used in those studies [7,12]. Phylogenetic analysis indicated that the majority of these fungal phylotypes belonged to two major phyla of Ascomycota and Basidiomycota with highly diversified fungal lineages within these individual phyla (multiple branches) (Figure 1). Similar findings were reported in a recent review in which the authors collected Figure 1. Maximum likelihood phylogenetic tree. 744 unique broad data sets of fungal small subunit ribosomal DNA (SSU fungal sequences derived from 30 marine fungal clone libraries are rDNA) and concluded the abundance of these two phyla [22]. aligned using Muscle v3.8 and undergo quality control in Mothur v1.25 Members of the phylum Ascomycota was found to be affiliated before used for phylogenetic tree generation. Maximum likelihood with the subphyla Pezizomycotina and Saccharomycotina, where- calculation is done in PhyML v3.0 corrected by model HKY85. The best as sequences of Basidiomycota belonged to three subphyla i.e. tree was returned by searching tree topology using subtree pruning and regrafting (SPR) algorithm starting with 5 random trees. Agaricomycotina, Pucciniomycotina and Ustilaginomycotina. In doi:10.1371/journal.pone.0101523.g001 addition to these two major phyla, two additional clades were not previously described in marine fungi (Figure 1 and Table S3 in File (p = 0.005) (Figure 2). Our results clearly support that planktonic S1). These two clades were deeply branched. The majority of the fungi play an important role in ocean nutrient cycling. OTUs had no affiliation to reported fungal sequences in the current database but had low sequence similarity to some Phylogenetic affiliation of fungal

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