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A New Chytridiomycete Fungus Intermixed with Crustacean Resting Eggs in a 407- Million-Year-Old Continental Freshwater Environment

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A New Chytridiomycete Fungus Intermixed with Crustacean Resting Eggs in a 407- Million-Year-Old Continental Freshwater Environment A new chytridiomycete fungus intermixed with crustacean resting eggs in a 407- million-year-old continental freshwater environment Strullu-Derrien, Christine; Gora, Tomasz; Longcore, Joyce E.; Olesen, Jørgen; Kenrick, Paul; Edgecombe, Gregory D. Published in: P L o S One DOI: 10.1371/journal.pone.0167301 Publication date: 2016 Document version Publisher's PDF, also known as Version of record Document license: CC BY Citation for published version (APA): Strullu-Derrien, C., Gora, T., Longcore, J. E., Olesen, J., Kenrick, P., & Edgecombe, G. D. (2016). A new chytridiomycete fungus intermixed with crustacean resting eggs in a 407-million-year-old continental freshwater environment. P L o S One, 11(12), [e0167301]. https://doi.org/10.1371/journal.pone.0167301 Download date: 08. apr.. 2020 RESEARCH ARTICLE A New Chytridiomycete Fungus Intermixed with Crustacean Resting Eggs in a 407-Million- Year-Old Continental Freshwater Environment Christine Strullu-Derrien1*, Tomasz Goral2, Joyce E. Longcore3, Jørgen Olesen4, Paul Kenrick1, Gregory D. Edgecombe1 1 Department of Earth Sciences, The Natural History Museum, Cromwell Road, London, United Kingdom, 2 Imaging and Analysis Centre, The Natural History Museum, Cromwell Road, London, United Kingdom, 3 School of Biology and Ecology, University of Maine, 5722 Deering Hall, Orono, ME, United States of a11111 America, 4 Natural History Museum, University of Copenhagen, Universitetsparken, Denmark * [email protected] Abstract The 407-million-year-old Rhynie Chert (Scotland) contains the most intact fossilised OPEN ACCESS remains of an early land-based ecosystem including plants, arthropods, fungi and other Citation: Strullu-Derrien C, Goral T, Longcore JE, microorganisms. Although most studies have focused on the terrestrial component, fossil- Olesen J, Kenrick P, Edgecombe GD (2016) A New Chytridiomycete Fungus Intermixed with ised freshwater environments provide critical insights into fungal-algal interactions and the Crustacean Resting Eggs in a 407-Million-Year-Old earliest continental branchiopod crustaceans. Here we report interactions between an enig- Continental Freshwater Environment. PLoS ONE 11 matic organism and an exquisitely preserved fungus. The fungal reproductive structures are (12): e0167301. doi:10.1371/journal. intermixed with exceptionally well-preserved globular spiny structures interpreted as bran- pone.0167301 chiopod resting eggs. Confocal laser scanning microscopy enabled us to reconstruct the Editor: Jae-Hyuk Yu, University of Wisconsin fungus and its possible mode of nutrition, the affinity of the resting eggs, and their spatial Madison, UNITED STATES associations. The new fungus (Cultoraquaticus trewini gen. et sp. nov) is attributed to Chytri- Received: September 13, 2016 diomycota based on its size, consistent formation of papillae, and the presence of an internal Accepted: November 4, 2016 rhizoidal system. It is the most pristine fossil Chytridiomycota known, especially in terms of Published: December 14, 2016 rhizoidal development and closely resembles living species in the Rhizophydiales. The Copyright: © 2016 Strullu-Derrien et al. This is an spiny resting eggs are attributed to the crustacean Lepidocaris rhyniensis, dating branchio- open access article distributed under the terms of pod adaptation to life in ephemeral pools to the Early Devonian. The new fungal interaction the Creative Commons Attribution License, which suggests that, as in modern freshwater environments, chytrids were important to the mobili- permits unrestricted use, distribution, and sation of nutrients in early aquatic foodwebs. reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Introduction Funding: This work was supported by a Marie Direct fossil evidence of fungal interactions and fungal diversity in general is relatively limited, Curie Intra-European Fellowship for Career principally because investigation of the fossil record is underdeveloped [1]. Paradoxically, one Development (SYMBIONTS GA±2011±298735) and a FP7 SYNTHESYS grant (NL-TAF 3245) of the of the few well-studied fossil fungi sites is also one of the oldest. The 407-Myr-old Rhynie European Commission to C.S.-D for data collection Chert (Scotland, UK) preserves its biotic components in exquisite detail [2]. The cherts formed and analysis. from erupted hydrothermal fluids that periodically inundated vegetation on a low-energy PLOS ONE | DOI:10.1371/journal.pone.0167301 December 14, 2016 1 / 14 Devonian Fungal Foodweb Competing Interests: The authors have declared alluvial plain formed by a braided river channel. Minor variations in topology across the flood- that no competing interests exist. plain gave rise to habitats that ranged from terrestrial to fully freshwater [3]. Fungal interac- tions in the terrestrial environments include the earliest evidence of plant parasitism and symbiosis (e.g. [4±8]), whilst interactions in freshwater involve fungi and algae [9, 10]; the lat- ter also contain the earliest continental branchiopod crustaceans [11±13]. Fossil remains of Chytridiomycota (chytrids) and Blastocladiomycota (blastoclads) have been reported from both environments [8±10, 14±20]. These true Fungi are early diverging lineages in the fungal tree of life that reproduce with motile spores (zoospores). The body or thallus is formed by organs of reproduction (zoosporangia and resting sporangia) arising from a vegetative part consisting of rhizoids. The most prominent morphological feature of the thallus is the zoospo- rangium, a sac-like structure bearing one or more discharge tubes or exit papillae. Zoosporan- gia are thin-walled whereas resting sporangia are thick-walled structures that may germinate to produce a sporangium after a dormant period. Fossil remains of chytrids (Chytridiomycota and Blastocladiomycota) have been reported from both environments [8±10, 14±20]. Chytrids are true Fungi that are an early diverging lineage in the fungal tree of life [21, 22]. Today, chy- trids and blastoclads are ubiquitous, occurring in diverse habitats from the tropics to the arctic regions [23]. They develop in terrestrial habitats [24] as saprotrophs or obligate parasites of plants [22]. They are the dominant parasites of algae and plankton in aquatic ecosystems, and recently they have been recognised as playing a fundamental role in zooplankton production and aquatic foodwebs [25]. Here we document a new freshwater chytrid from the Rhynie Chert interacting with structures of unknown affinity. Intermixed with the fungal reproductive structures are spinose fossils that we identify as resting eggs of the branchiopod crustacean Lepidocaris rhyniensis, the post-embryonic stages of which are abundant and well-preserved in the slides. Results extend our knowledge of the early fossil record of Fungi, providing compel- ling evidence of a conserved trophic role for chytrids in one of the earliest well-documented freshwater communities. Materials and Methods We examined historical collections of Rhynie Chert preparations made during the early part of the 20th century primarily to document the fossil plants. We studied a series of thin sections housed at the Natural History Museum London (NHMUK V 15641, NHMUK V 16429, NHMUK V16432, NHMUK V16433, NHMUK V 67866, NHMUK V67867, NHMUK V 67910), the National Museum of Scotland, Edinburgh (NMS G.1925-9-11, NMS G.1925-9-14), and Naturalis Biodiversity Center, Leiden (Netherlands) (RH 585). Zeiss Axioskop and Nikon Eclipse LV100ND compound microscopes were used to examine and photograph specimens with transmitted light. Depth of field was enhanced through z-stack montage. Confocal Laser Scanning Microscopy (CLSM) is a form of optical microscopy that yields high resolution images of minute objects [26±28]. This method has been used for imaging chy- trid sporangia and spores in cellulose acetate peels [27] and plant and fungal tissues in thin sec- tion from the Rhynie Chert [8]. Using the latter as a proof of concept, we performed analyses on a larger scale to document the fungal association here described. The presence of Canada Balsam, which was used as a mounting medium, sometimes caused problems of significant background autofluorescence, but we were able to eliminate this by adjusting the setting and time of acquisition of data, and by applying correction parameters. In addition to the opacity of some of the fossil structures, which can inhibit fluorescence, the major difficulties encoun- tered were (1) the generally thicker petrographic thin sections, (2) the fact that the section of chert was not perfectly flat or equally thick across and (3) the variable thickness and quality of the glass coverslips. We were able to work around this problem using 40× and 60× lenses and PLOS ONE | DOI:10.1371/journal.pone.0167301 December 14, 2016 2 / 14 Devonian Fungal Foodweb by zooming on the object. CLSM represents an accurate, non-destructive methodology for col- lecting 3D morphological data on thin sections of chert. We acquired confocal images with a Nikon A1-Si laser-scanning confocal microscope. Images were recorded with pixel dimensions of 0.31 μm. Autofluorescence of the samples was excited with the following laser lines: 405-nm line of 100 mW cube laser (Coherent Inc., USA, http://www.coherent.com), 488-nm line of 50 mW sapphire laser (Coherent Inc., USA), 561-nm line of 50 mW sapphire laser (Coherent Inc., USA) and 640-nm line of 40 mW cube
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