Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives Sofia Duarte a, * , Felix B € arlocher b , Cl audia Pascoal a , Fernanda C assio a a Centre of Molecular and Environmental Biology (CBMA), Department of Biology, University of Minho Campus de Gualtar, 4710-057 Braga, Portugal b Department of Biology, Mount Allison University, Sackville, New Brunswick E4L 1G7, Canada article info Article history: Received 2 March 2015 Received in revised form 26 May 2015 Accepted 5 June 2015 Available online xxx Keywords: Aquatic hyphomycetes Biogeography Phylogeography Metagenomics Morphospecies Genetic diversity Next-generation sequencing abstract Since Ingold's (1942) initial description, mycologists have been interested in deciphering global distri- bution patterns of aquatic hyphomycetes, a group of fungi that play a key role in plant-litter decom- position in freshwaters. However, many questions remain largely unanswered. In this review, we used distribution data of morphospecies from studies throughout the world in an attempt to better under- stand the magnitude of global species richness, patterns of biodiversity and the extent of cosmopoli- tanism versus endemism. Sampling efforts have varied among geographic regions, and correlate significantly with species richness. Community similarity decreased with geographic or latitudinal dis- tance. Species richness was highest at mid-latitudes (temperate streams), and high community simi- larities were found between geographically distant locations in similar climatic zones. Studies relying on morphotypes have undoubtedly provided relevant information on the geographic distribution of aquatic hyphomycetes. However, metagenomic approaches combining taxonomic, phylogenetic and functional diversity in coordinated surveys will be the best option to better decipher diversity patterns of these fungi and their functional roles at a global scale. © 2015 Elsevier Ltd and The British Mycological Society. All rights reserved. 1. Introduction Fungi are widely distributed across all biomes and play a major role in the recycling of organic matter with more than 600 species reported from freshwaters (Wong et al., 1998; Shearer et al., 2007). Ingoldian fungi or aquatic hyphomycetes abound in well-aerated waters and are regarded as the dominant microbial decomposers of leaves decaying in streams (B€ arlocher, in this issue). Members of this ecologically defined group regularly sporulate under water, and have large conidia (often spanning more than 50 mm) of two predominant shapes: branched and often tetraradiate or multi- radiate (stauroid), and sigmoid or worm-like (scolecoid) (Gulis et al., 2005; Shearer et al., 2007)(Fig. 1). Much of our knowledge on aquatic hyphomycete diversity in freshwaters emerges from species classification based on their characteristic conidial shapes. Though slightly heavier than water, conidia are readily trapped in foam or scum, which accumulates in streams (Ingold, 1975). Con- idia can also be sampled from the water column by filtration or from naturally colonized submerged substrata (e.g. leaves, twigs) and substrate baits after inducing sporulation in the laboratory (Gulis et al., 2005). De Wildeman (1893, 1894, 1895) was the first to recognize some of the typical conidial forms of aquatic hyphomycetes and described species of several genera (Clavariopsis, Lemonniera and Tetracladium)(Fig. 1). However, these fungi only gained relevance nearly half a century later when Ingold (1942) described 16 forms of conidia and traced them back to mycelia on decaying alder leaves in a stream near Leicester, in England. In the first of many papers devoted to aquatic hyphomycetes, Ingold (1942) wrote: “My ob- servations on aquatic hyphomycetes have been limited, so far, to the immediate neighbourhood of Cropston in Leicestershire, but it is of interest to know if they are of wide occurrence”. In subsequent years, he found identical or similar spores in samples from many regions in Britain (Ingold, 1943a,b), and other parts of the world, including Europe (e.g. Switzerland: Ingold, 1949), Africa (Nigeria: Ingold, 1956, 1959; Uganda and Zimbabwe: Ingold, 1958; Swaziland: Ingold, 1973), North America (Canada: Ingold, 1960) and Caribbean Islands (e.g. Jamaica: Hudson and Ingold, 1960), thus demonstrating the world-wide occurrence of aquatic hyphomy- cetes. Studies by other researchers confirmed their global distri- bution (e.g. California: Ranzoni, 1953; Japan: Tubaki, 1957; eastern * Corresponding author. E-mail address: [email protected] (S. Duarte). Contents lists available at ScienceDirect Fungal Ecology journal homepage: www.elsevier.com/locate/funeco http://dx.doi.org/10.1016/j.funeco.2015.06.002 1754-5048/© 2015 Elsevier Ltd and The British Mycological Society. All rights reserved. Fungal Ecology xxx (2015) 1e10 Please cite this article inpress as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal Ecology (2015), http://dx.doi.org/10.1016/j.funeco.2015.06.002
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Biogeography of aquatic hyphomycetes: Current knowledge andfuture perspectivesSoa Duarte a, *, Felix Barlocher b, Cl
audia Pascoal a, Fernanda C
assio aaCentre of Molecular and Environmental Biology (CBMA), Department of Biology, University of Minho Campus de Gualtar, 4710-057 Braga, PortugalbDepartment of Biology, Mount Allison University, Sackville, New Brunswick E4L 1G7, Canadaarti cle i nfoArticle history:Received 2 March 2015Received in revised form26 May 2015Accepted 5 June 2015Available online xxxKeywords:Aquatic hyphomycetesBiogeographyPhylogeographyMetagenomicsMorphospeciesGenetic diversityNext-generation sequencingabstractSince Ingold's (1942) initial description, mycologists have been interested in deciphering global distri-bution patternsofaquatichyphomycetes, agroupoffungithatplay akeyroleinplant-litter decom-position in freshwaters. However, many questions remain largely unanswered. In this review, we useddistributiondata of morphospecies from studiesthroughout the world in an attempt to better under-standthemagnitudeofglobalspeciesrichness, patternsofbiodiversity andtheextentofcosmopoli-tanismversus endemism. Sampling efforts have varied among geographic regions, and correlatesignicantly with species richness. Community similarity decreased with geographic or latitudinal dis-tance. Speciesrichnesswashighestatmid-latitudes(temperatestreams), andhighcommunitysimi-larities were found between geographically distant locations in similar climatic zones. Studies relying onmorphotypes have undoubtedly provided relevant information on the geographic distribution of aquatichyphomycetes. However, metagenomicapproaches combining taxonomic,phylogenetic and functionaldiversityincoordinatedsurveyswillbethebestoptionto better decipherdiversitypatternsofthesefungi and their functional roles at a global scale. 2015 Elsevier Ltd and The British Mycological Society. All rights reserved.1. IntroductionFungi are widely distributed across all biomes and play a majorrole in the recycling of organic matter with more than 600 speciesreported from freshwaters (Wong et al., 1998; Shearer et al., 2007).Ingoldianfungioraquatichyphomycetesaboundin well-aeratedwaters and are regarded as the dominant microbial decomposersof leaves decaying in streams (B arlocher, in this issue). Members ofthisecologicallydenedgroupregularlysporulateunderwater,and have large conidia (often spanning more than 50mm) of twopredominant shapes: branchedandoftentetraradiateor multi-radiate(stauroid), andsigmoidor worm-like(scolecoid) (Guliset al., 2005; Shearer et al., 2007) (Fig. 1). Much of our knowledgeonaquatichyphomycetediversityinfreshwatersemergesfromspecies classication based on their characteristic conidial shapes.Though slightly heavier than water, conidia are readily trapped infoam or scum, which accumulates in streams (Ingold, 1975). Con-idiacanalsobesampledfromthewatercolumnbyltrationorfrom naturally colonized submerged substrata (e.g. leaves,twigs)andsubstratebaitsafterinducingsporulationinthelaboratory(Gulis et al., 2005).De Wildeman (1893, 1894, 1895) was the rst to recognize someof the typical conidial forms of aquatic hyphomycetes anddescribedspeciesofseveralgenera(Clavariopsis, LemonnieraandTetracladium) (Fig. 1). However, these fungi only gained relevancenearly half a century later when Ingold (1942) described 16 forms ofconidia and traced themback to mycelia on decaying alder leaves inastreamnearLeicester, inEngland. Intherstof manypapersdevotedtoaquatichyphomycetes, Ingold(1942)wrote: Myob-servations on aquatic hyphomycetes have been limited,so far,tothe immediate neighbourhood of Cropston in Leicestershire, but itis of interest to knowif they are of wide occurrence. In subsequentyears, he found identical or similar spores in samples from manyregions in Britain (Ingold, 1943a,b), and other parts of the world,including Europe (e.g. Switzerland: Ingold, 1949),Africa (Nigeria:Ingold, 1956, 1959; Uganda and Zimbabwe: Ingold, 1958;Swaziland: Ingold, 1973), North America (Canada: Ingold, 1960) andCaribbeanIslands(e.g. Jamaica: HudsonandIngold, 1960), thusdemonstratingtheworld-wideoccurrenceof aquatichyphomy-cetes. Studiesbyotherresearchersconrmedtheirglobaldistri-bution (e.g. California: Ranzoni, 1953; Japan: Tubaki, 1957; eastern *Corresponding author.E-mail address: [email protected] (S. Duarte).Contents lists available at ScienceDirectFungal Ecologyj ournal homepage: www. el sevi er. com/ l ocat e/ f unecohttp://dx.doi.org/10.1016/j.funeco.2015.06.0021754-5048/ 2015 Elsevier Ltd and The British Mycological Society. All rights reserved.Fungal Ecology xxx (2015) 1e10Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, FungalEcology (2015), http://dx.doi.org/10.1016/j.funeco.2015.06.002 USA: Petersen1962, 1963a,b; Scandinavia: Nilsson, 1958, 1964;South Africa: Greathead, 1961; Australia: Cowling and Waid, 1963;Cuba: Marvanova and Marvan, 1969 and Malaysia: Nawawi, 1985).Comparedtootherfreshwaterfungi, thedistributionof aquatichyphomycetes is relatively well studied and several data compila-tions exist based on morphospecies (taxonomy based on morpho-logical differences of the conidia) (e.g. Ingold, 1975; Webster andDescals, 1981; Marvanov a, 1997; Santos-Flores andBetancourt-L opez, 1997;Gulisetal., 2005), althoughstudiesintropicallati-tudes have been less common (e.g. Sridhar et al., 1992; Goh, 1997;Marvanova, 1997). Comparablecommunities exist intemperatezones on both sides of the equator; streams closer to the equatorare represented by a characteristic tropical mycoora, whichnevertheless contains many species common to temperate zones(Wood-Eggenschwiler and B arlocher, 1985). In fact, many species ofaquatic hyphomycetes have been found in streamfoam collected indifferentpartsof theworld(Ingold, 1975;WebsterandDescals,1981), suggestingthatthedistributionof aquatichyphomycetesmight followthe hypothesis of Baas Becking (1934). This hypothesispostulates, withrespect tomicrobes, that everythingisevery-whereandthatsmall organisms(