Fungal Diversity Classification of marine Ascomycota, anamorphic taxa and Basidiomycota Jones, E.B.G.1*, Sakayaroj, J.1, Suetrong, S.1, 3, Somrithipol, S.1 and Pang, K.L.2 ¹Bioresources Technology Unit, Phylogenetics Laboratory, National Center for Genetic Engineering and Biotechnology, 113 Paholyothin Road, Khlong 1, Khlong Luang, Pathum Thani 12120, Thailand 2Institute of Marine Biology, National Taiwan Ocean University, No. 2 Pei-Ning Road, Keelung 20224, Taiwan 3Department of Microbiology, Faculty of Science, Prince of Songkla University, Hat Yai, Songkhla, 90112, Thailand. Jones, E.B.G., Sakayaroj, J., Suetrong, S., Somrithipol, S. and Pang, K.L. (2009). Classification of marine Ascomycota, anamorphic taxa and Basidiomycota. Fungal Diversity 35: 1-187. A comprehensive classification of the filamentous marine fungi is outlined, with reference to recent molecular phylogenetic analyses. The classification includes 530 species (in 321 genera) to order level: Ascomycota 424 species (in 251 genera), anamorphic fungi 94 species (in 61 genera) and Basidiomycota 12 species (in 9 genera). The Halosphaeriales is the largest order of marine fungi with 126 species in 53 genera, of which 35 are monotypic. Several taxa are of uncertain position and cannot be assigned to any higher taxonomic ranks. The decadel index shows that most marine fungi were described in the period 1980-1989 (135) and 1990-1999 (156), with 43 new species and 25 new genera from the past eight years. Keys are provided to the major taxa, genera and species. One new species is described in this paper. Key words: fungal classification, marine fungi, molecular phylogeny, rDNA, new taxa Article Information Received 1 December 2008 Accepted 23 December 2008 Published online 24 March 2009 *Corresponding author: E.B.G. Jones; e-mail: [email protected] Introduction reliable recent figure is that of Hyde et al. (2000) who listed 444 “higher” obligate marine Although a few synoptic keys are fungi. However, a number of taxa were not available for the identification of obligate listed, while a further 43 new species in ten marine fungi (Kohlmeyer and Volkmann- new genera have been described over the past Kohlmeyer, 1991a; Hyde et al., 2000), there eight years. A further 15 new genera have been has been no attempt to present a classification introduced to accommodate species rejected for them since the book of Kohlmeyer and from existing genera. Other species not Kohlmeyer (1979). This monograph addresses previously regarded as marine are included in this issue. this monograph. The total now stands at 530 The number of marine fungi described and new taxa continue to be described from has increased dramatically since the pioneer this habitat. study of Barghoorn and Linder (1944) on ligni- Kohlmeyer and Kohlmeyer (1979) stated colous species. Currently some 1,500 names that: “the decrease of new descriptions of can be found in the literature, but many of marine fungi during the period 1970-1977 these are inadequately described, or may be indicates that the most common species have facultative terrestrial species or synonyms of been named and that considerable additions of existing taxa (Jones and Mitchell, 1996). new taxa in the future are unlikely.” However, However, Schaumann (pers. comm.) estimates as new substrata and geographical locations are there are some 6,000 marine species, but this being examined for fungi, the number of new figure is not supported by data. The most species continues to rise (Fig. 1): 135 in 1980- 1 Fig. 1. Decadel increase in the number of marine fungi. 1989; 156 in 1990-1999 and 43 already marine Ascomycota: Decorospora gaudefroyi recorded for the period 2000-2008. This is (as Pleospora gaudefroyi) (Yusoff et al., certainly noticeable for mangrove species (42 1994b), Julella avicenniae (Au et al., 1999a) species in Kohlmeyer and Kohlmeyer, 1979; and the genus Massarina (Au et al., 2001; over 170 in Hyde et al., 2000), and tropical Read et al., 1994, 1997a, b). Although locations continue to yield a wide range of ultrastructural characters helped in the new taxa (Jones et al., 2006; Koch et al., delineation of a number of genera (e.g. 2007). Kis-Papo (2005) has reviewed data on Corollospora) others were found to be more the number of marine fungi and settles on 467 difficult to resolve (e.g. Halosarpheia). species. Over the last decade, the use of Identification and classification of the molecular techniques to examine the phylo- marine higher fungi have followed traditional geny of organisms has advanced considerably avenues of the evaluation and significance of (Spatafora and Blackwell, 1994). Molecular morphological characters at the light micro- techniques have also been applied to examine scope level. For the Ascomycota, ultra- the relationships of a number of marine taxa at structural characters at the transmission and the ordinal level and at the genus/species level. scanning electron microscope levels have also The earliest study was on the phylogeny of been used (Jones, 1995). These were Halosphaeriopsis mediosetigera (as a repre- specifically applied to ascospore appendage sentative of the Halosphaeriales), and the ontogeny of the Halosphaeriales, where Microascales, with both orders sharing a delineation of genera was questioned, e.g. common ancestor (Spatafora and Blackwell, Corollospora (Kohlmeyer, 1972a; Jones et al., 1994). This relationship has also been 1983a), and Ceriosporopsis (Johnson et al., supported by other studies (Chen et al., 1999; 1987). Kong et al., 2000). Exploratory studies using TEM and Spatafora et al. (1998) showed that the SEM were also used for selected bitunicate genus Lulworthia did not group within the 2 Fungal Diversity Halosphaeriales clade, also noted by Campbell Origin of marine fungi (1999) and Chen et al. (1999). Subsequently, Kohlmeyer et al. (2000) erected the new order Many theories have been advanced to Lulworthiales to accommodate the genera account for the origin of marine fungi, and in Lindra and Lulworthia, while Inderbitzin et al. particular the ascomycetes, the Floridean (2004) showed that the genera Spathulospora hypothesis being the favoured one (Denison and Haloguignardia had affinities with the and Carroll, 1966; Kohlmeyer, 1975a; Lulworthiales. Campbell et al. (2005) erected Demoulin, 1985). Spathulospora was two monotypic genera within the order to considered to be closely related to the accommodate Lulworthia-like species that did Laboulbeniales, a group in turn thought to be not form a monophyletic group with related to the Rhodophyta (Kohlmeyer, 1973b). Lulworthia fucicola, the type species Furthermore, Kohlmeyer (1975a) suggested (neotypified by Campbell, 2005). Many taxa in that Spathulospora, with its marine occurrence the Halosphaeriales have also been sequenced and as a parasite of the red alga Ballia, “was to infer phylogenetic relationships between close to the hypothetical ancestor of morphologically similar taxa. Studies by Kong Ascomycetes”. However, in a little cited paper, et al. (2000) and Abdel-Wahab et al. (2001b) Walker et al. (1979) questioned the view that confirmed the polyphyly of the genus Halo- Spathulospora belonged to an ancestral group, sarpheia and this led to the erection of a or along with the Laboul-beniales and number of new genera (Campbell et al., 2003; Uredinales, could be considered “living Pang et al., 2003a, b). fossils”. Many genera in the Ascomycota have That marine fungi are an ecological group not been referred to a family or even an order has never been in dispute, but did they evolve (Hawksworth et al., 1995; Kirk et al., 2001). in the sea or were they secondly adapted to life However, the use of molecular techniques has in the marine milieu? While the latter view has enabled the resolution of a number of genera. gained in acceptance, there has been little Tam et al. (2003) have shown that the solely evidence to support it. Spatafora et al. (1998) known marine bitunicate genera, Aigialus, however have advanced the discussion by Helicascus, Julella and Paraliomyces, with demonstrating that the Halosphaeriales at least unknown ordinal affinity, can now be has made the transition from terrestrial to classified in the Pleosporales. Similar marine habitats with the consequent loss of resolution is possible for the basidiomycetes dehiscing asci. They also concluded that this Calathella, Digitatispora, Halocyphina, was not a solitary episode, as the Lulworthiales Mycaureola and Nia (Binder et al., 2001; was also a transitional group, arising indepen- Hibbett and Binder, 2001, 2002; Binder et al., dently of the Halosphaeriales (Kohlmeyer et al., 2006). However, many taxa remain to be 2000). examined before their assignment to an order Sakayaroj (2005) and Schoch et al. (2006) can be made. In this monograph we have indicated that within the unitunicate reviewed the published literature so as to ascomycetes seven and three lineages, propose the best taxonomic assignment for respectively, have migrated into the sea. “obligate” marine fungi. However, conflict Furthermore five lineages of marine bitunicate may arise between traditional classifications ascomycetes are also indicated from analyses of and the need to incorporate phylogenetic molecular data (Suetrong et al., unpublished analysis, as in the case of the marine data) and may be intermediate forms with many Basidiomycota. retaining active ascospore discharge. The latter We have supplied a key within each group is particularly prevalent in mangrove genus with more than one species, and added habitats where ascus discharge can take place notes on others that may be useful for further during the intertidal period. Likewise, other research and understanding of their ecology. groups can be shown to have evolved from 3 terrestrial to marine habitats: at least three There is no data to indicate when marine lineages of the Basidiomycota (Binder et al., fungi evolved from terrestrial species, 2006), as well as ascomycetes with although Vijaykrishna et al. (2006) predicted cleistothecial ascomata, but for which no that fungi became adapted to freshwater some phylogenetic data is available: e.g. Biflua and 390 million years ago. Many lineages of Marisolaris (Koch and Jones, 1989).