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Yeast forms dominate fungal diversity in the deep oceans David Bass1, Alexis Howe1, Hannah Barton1, Nick Brown2, Maria Demidova 1, Harlan Michelle1, Lily Li1, Holly Sanders1, Sarah Watkinson2, Simon Willcock1, Thomas A. Richards3. 1 Department of Zoology, University of Oxford, The Tinbergen Building, South Parks Road, Oxford, OX1 3PS, UK 2 Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, UK 3 School of Biosciences, University of Exeter, Devon, EX4 4QD, UK SUPPLEMENTARY ONLINE MATERIAL Supplementary Table 1. Provenance of eDNA samples and relative recovery of fungal and non- fungal sequences. 18S rDNA library Ocean No. of No. % % % DNA clones fungal non- randomly- extractions successf funga ligated / PCR ully l DNA reactions sequence fragments for cloning d Deep anoxic (1575m) (2 Guaymas Bay, 3/6 60 25 7 68 libraries) Gulf of California Colonization module Mid Atlantic 1/4 21 0 33 (E. 67 (1,695m) (1 library) coli) Drake Passage (250m & Southern Ocean 2/6 35 44 34 23 500m) (2 libraries) Drake Passage (2,000m Southern Ocean 2/6 34 38 3 59 & 3,000m) (2 libraries) Rainbow metal-rich Mid Atlantic 1/4 20 65 0 35 sediment (2,264m) (1 library) Titanic site (3,000m & Mid Atlantic 2/6 35 97 3 0 3,700m) (1 library) Bismarck site (3,000m & Mid Atlantic 2/6 34 91 3 6 4000m) (1 library) Supplementary Table 2. Provenance of fungal 18S-types detected in this study. Code Taxonomic Bismarck Titanic Rainbow Drake Anaerobic Drake Close relative occurs in other deep- (figure 1, affiliation site site sediment Passage . bacterial Passage sea studies 2 & 3) (3000m & (3000m & (2,264m) (2000m & mat (250m & 4000m) 3700m) 3000m) (1575m) 500m) DB39 Unresolved NF KD12 Chytridiaceae NF CE2 Ustilaginomycete (Edgcomb et al. 2002; López- García et al. 2007; López-García et al. 2003) CK2 Ustilaginomycete (Edgcomb et al. 2002; López- García et al. 2007; López-García et al. 2003) DB7 Ustilaginomycete (Edgcomb et al. 2002; López- (partial sequence – García et al. 2007; López-García et see figure 4) al. 2003) KM10 Ustilaginomycete (Edgcomb et al. 2002; López- García et al. 2007; López-García et al. 2003) HC8 Hymenomycete NF HC7 Hymenomycete NF JJ12 Hymenomycete NF NB16 Hymenomycete NF JJ14 Hymenomycete NF MD13 Hymenomycete NF JJ11 Urediniomycete NF MD7 Urediniomycete NF JJ15 Saccharomycotina NF LL7 Saccharomycotina NF MH1 Saccharomycotina NF KD10 Saccharomycotina NB13 Pezizomycotina (López-García et al. 2007) LL2 Pezizomycotina NF TOTALS 8 11 3 3 4 4 NF = not found in previous general eukaryotic analyses Supplementary table 3. Identifying putative biology of fungal sequences detected in our marine samples and other deep-sea samples. Non-fungal sequences (e.g. KD14) and sequences that could not be placed with known fungal species with strong bootstrap support of 90% or more were not included (e.g. DB39). Possibility of yeast lifecycle Presence in Deep / Shallow Possibility of filamentous (hyphaea) lifecycle stage Possibility of f zoospore Possibility of parasitism Max. identity % BLAST e-value clone libraries GenBank Accession stage Known Clone numbers Description species (and reference) KD12 Chytridium 0.0 92 AY032608 1/0 Y Y The phylogenetic position of KD12 is relatively distant from polysiphoniae Chytridium and Chytriomyces (figure 1). Chytridium are typically parasitic on other fungi, on algae or protozoa and C. polysiphoniae is a pathogen of marine macroalgae (marine brown algae) (Muller et al. 1999) CE2 Malassezia 0.0 95 2/1 Y Y Y CE2 branches strongly with M. furfur but forms a distinct branch BOH2_E furfur 0.0 95 DQ504358 - (figure 2). Ustilginomycete lipophilic yeast commonly colonizes K4_20 (AY083223) (López- skin of humans and animals. Possibly pathogenic and García et al. implicated as causative agent of seborrhoeic dermatitis and 2007) dandruff (Webster & Weber 2007). Hyphae are formed in certain conditions (Webster & Weber 2007). Detected independently in multiple deep-sea environmental gene libraries (López-García et al. 2007). CK2 Malassezia 0.0 95 2/0 Y Y Y See CE2 for description (Edgcomb et al. 2002; López-García et BOH3_E furfur 0.0 94 DQ504359 al. 2007; López-García et al. 2003; Webster & Weber 2007) K4_7 (AY083223) (López- García et al. 2007) LC23_5E 0.0 94 DQ504335 P_14 (López- García et al. 2007) BAQA52 0.0 94 AF372708 (Dawson & Pace 2002) WIM108 0.0 95 AM114819 (Moon-van der Staay et al. 2006) KM10 0.0 95 4/1 AT9-6 0.0 94 AF530542 (López- García et al. 2003) A1_E022 0.0 94 AY046689 (Edgcomb et al. 2002) PAT6_EK 0.0 94 DQ504360 5_11 (López- García et al. 2007) HC8 Cryptococcus 0.0 95 1/0 Y Y HC8 groups within a cluster of Cryptococcus sequences with carnescens strong support (figure 2). Cryptococcus carnescens has been (DQ645520) recently elevated to species after previously being known as a and Taphrina strain of Cryptococcus laurentii (isolated from plants, soil and maculans clinical specimens) (Takashima et al. 2003). Taphrina (AB000953) maculans found in subantarctic water of Pacific Ocean, Black (species and North Sea (Jones 1976) causaul agent of brown leaf spot name disease (Upadhyay & Pavgi 1979) transmitted by air borne probably miss infection (hosts: turmeric - Curcuma domestica, Zingiber spp.). identified) The fungus has a strictly phytoparasitic filamentous state that gives rise to asci on the infected plant tissue (i.e. the teleomorph) and a saprobic yeast state that results from budding of the ascospores (Inacio et al. 2004). Evidence from molecular and phenotypic characters suggests T. maculans should be excluded from the archaeascomycetes lineage as it groups within the basidiomycetes with strong support ((Sjamsuridzal et al. 1997) and figure 2). HC7 Cryptococcus 0.0 95 1/0 Y Y HC7 groups within a cluster of Cryptococcus sequences with albidus strong support (figure 2). Cream, mucoid colonies; vegetative (AB032617) reproduction by budding; no filaments; no sexual reproductions and (Barnett et al. 1990). Found in air, a range of marine Cryptococcus environments (Jones 1976), wine, sake-moto, soil, leaves, vishniacii cheese, water, effluent of a pulp mill, man and other mammals (AB032657) (Barnett et al. 1990). JJ12 Filobasidium 0.0 95 1/0 Y Y Y JJ12 groups strongly within a cluster of Filobasidium (figure 2). uniguttulatum Filobasidium form cream mucoid colonies; vegetative (AB032664), reproduction by budding; filaments, none or septate hyphae; globisporum sexual reproduction by basidia (Barnett et al. 1990). (AB075546) Uniguttulatum is found on man and other mammals (Barnett et and floriforme al. 1990). Globisporum found in dead florets of Erianthus (D13460) giganteus in South Carolina (Barnett et al. 1990) and in the deep meromictic Lake Pavin (Lefevre et al. 2007). Floriforme found on grain and on florets of Erianthus giganteus (plume grass) and the skeleton of coral (Domart-Coulon et al. 2004) and is unable to grow anaerobically (Visser et al. 1990). Characteristic of this genus are the elongated thick-walled sporophores bearing apically conidia or spores like a "flower head" which were interpreted as basidia with basidiospores (Rodrigues de Miranda 1972). NB16 Antrodia 0.0 99 1/0 Y Y Antrodia are polypore fungus (Polyporaceae family) which form variiformis resupinate or bracket-shaped basidiocarps and numerous (AY336782) fiberous hyphae (dimitic hyphal system) with clamped generative hyphae, aerial mycelium and in terrestrial environments is known to form fruiting bodies associated with brown rot (Kim et al. 2003). JJ14 Trichosporon 0.0 99 1/0 Y Y Y Based on SSU rDNA analyses (figure 2) the JJ14 sequence is pullulans a very close relative of T. pullulans. Trichosporon spp. include (AB001766) some occasional animal pathogens and a diversity of growth forms including hyphae, pseudohyphae, yeast cells, blastoconidia and arthroconidia (Webster & Weber 2007). T. pullulans is a widespread basidiomycete yeast (Hawksworth et al. 1995) and found in soil, water samples, vegetables, shown to be weakly or non-fermentative and having no sexual reproductive phase (Fell & Scorzetti 2004). MD13 Cystofilobasid 0.0 99 2/0 Y MD13 groups with C. infirmominiatum and C. macerans within ium a defined branch with strong support (figure 2). C. infirmominiatu infirmominiatum is a widespread basidiomycete yeast (found in m some marine samples) (Hawksworth et al. 1995). (C. macerans (AB032642) has been found in frozen samples from Iceland; found to be and cold-adapted and polyygalacturonase-producing (Birgisson et Cryptococcus al. 2003)). macerans (AB645524) JJ11 Rhodosporidi 0.0 99 2/0 Y Y Y JJ11 groups with R. diobovatum with moderate to strong um support (figure 2). Widespread basidiomycete yeast often diobovatum sampled in seawater (Hawksworth et al. 1995) a teleomorph of (AB073271) Rhodotorula glutinis (see Rhodotorula mucilaginosa - MD7 - below) although R. mucilaginosa is phylogenetically distinct from R. diobovatum (figure 2). R. diobovatum can form dikaryotic mycelium (Carlile et al. 2001) MD7 Rhodotorula 0.0 99 2/0 Y Y MD7 groups strongly with Rhodotorula sequences (figure 2). mucilaginosa Widespread basidiomycete yeast (Hawksworth et al. 1995) (DQ386306) found in air, soil, lakes, ocean water and dairy products can and colonize plants, humans, and other mammals (Biswas et al. Rhodotorula 2001). Colonies are rapid-growing, smooth, glistening or dull, sp. cream to pink or yellow/orange (Neofytos et al. 2007). Exhibit (DQ832199) unicellular blastoconidia and no hyphae (http://www.doctorfungus.org/thefungi/Rhodotorula.htm [Accessed 07/03/2007]). JJ15 Pichia 0.0 99 1/0 Y Y JJ15 groups strongly with Pichia (figure 3) that are fermentans characterised by budding cells with a few species producing (AB053241) hyphae (Webster & Weber 2007). Pichia fermentans, white to cream, butyrous colonies, vegetative reproduction by budding (ascospores) simple to elaborate pseudohyphae; evanescent asci (Jones 1976). Cosmopolitan and ubiquitous distribution (Webster & Weber 2007). LL7 Saccharomyc 0.0 99 0/1 Y LL7 branches very closely to Saccharomyces ascomycetes es cerevisiae (column 2 this table – figure 3). Cells are round to ovoid, 5– (Z75578) and 10m in diameter white to cream, butyrous colonies, vegetative Kazachstania reproduction by budding; filaments: non or simple zonata pseudohyphae; persistent asci, containing 1 to 12 smooth (AB198185) (Webster & Weber 2007). Saccharomyces cerevisiae is known from the surface of fruit but also isolated from marine waters from the Indian Equatorial, central water and Antarctic intermediate oceans (Jones 1976). Also found to be able to grow at high salt concentrations in lab experiments (Jones 1976). Kazachstania zonata isolated from leaf litter in southern Japan (Imanishi et al. 2007). Kazachstania types form single globose ascospore in an unconjugated and persistent ascus with multilateral budding (Limtong et al. 2007). MH1 Debaryomyce 0.0 98 3/0 Y MH1 branches closely to D. hansenii (figure 3). White to cream, s hansenii butyrous colonies, vegetative reproduction by budding; (EF428134) filaments: no or simple pseudohyphae; persistent asci containing 1 or 2 rough, round ascospores (Barnett et al. 1990). Debaryomyces hansenii is a cryotolerant, marine yeast, which can tolerate salinity levels up to 24%, found in: dairy, fruits, and many foods, mushrooms, air, flies, water, man and other mammals (Barnett et al. 1990). D. hansenii is the only species in the genus that is abundant in marine waters and has been isolated from all from all oceanic regions irrespective of water mass (Jones 1976). KD10 Candida 0.0 97 - 1/0 Y Y KD10 forms a long branch within a strongly supported cluster haemulonii, of Candida sequences (figure 3). White to cream, butyrous (AB013572) colonies, vegetative reproduction by budding; filaments: non or CYSGM- 0.0 95 AB275102 simple pseudohyphae; no sexual reproduction (Barnett et al. 19 (unpublished) 1990). Found in: marine environments, dolphins, fish (Haemulon sciurus) (Barnett et al. 1990) (http://www.mycology.adelaide.edu.au/Fungal_Descriptions/Ye asts/Candida/Candida_haemulonii.html [Accessed 07/03/2007]. Candida haemulonii has been reported from a few cases of fungemia (yeasts in the blood) but clinical isolations remain rare (Rodero et al. 2002). A1_E031 Cladosporium 0.0 99 AY046698 Y Y A1_E031 branches very close to Cladosporium cladosporioides cladosporioid (Edgcomb et (figure 3). Cladosporium is a pigmented fungal mould found es al. 2002) widely in air and rotten organic material. Some species are (DC678004) predominant in tropical and subtropical regions (De Hoog et al. 2000; Dixon & Polak-Wyss 1991) and have also been isolated from fish associated with infection (Bocklisch & Otto 2000). Conidia of Cladospoirium spp. are among the most abundant component of air spora (Gregory 1973). Cladosporium spp. are the causative agents of skin lesions, keratitis, onychomycosis, sinusitis and pulmonary infections (Collier et al. 1998; Pritchard & Muir 1987). Cladosporium spp. are generally olivaceous green to black from the front and black from the reverse and produce septate brown hyphae, erect and pigmented conidiophores, and conidia. Cladosporium cladosporioides has smooth conidium walls (Webster & Weber 2007). NB13 Aureobasidiu 0.0 99 1/0 Y Y Y Branches close to Aureobasidium with strong support (figure 3). m pullulans Aureobasidium pullulans is a ubiquitous saprotroph widely (DQ680682) distributed in both terrestrial and marine habitats (Webster & LC23_4E 0.0 99 DQ504331 Weber 2007). Characterised by a high growth rate and P_18 (López- abundant spore development, as well as great adaptation García et al. capabilities to unfavourable environmental conditions (Zvereva 2007) & Vysotskaya). Member of loosely grouped black yeast (melanized yeasts) (Kogej et al. 2005; Webster & Weber 2007). Isolated from an Okinawan marine sponge (Shigemori et al. 1998) and a bivalve Modiolus modiolus, (Zvereva & Vysotskaya). Opportunistic human pathogen of brain and other organs (Webster & Weber 2007). A2_E003 Neurospora 0.0 99 AY046715 Y A2_E003 LL7 branches very closely to Neurospora crassa crassa (Edgcomb et (figure 3). Many Neurospora species grow in humid tropical and (X04971) al. 2002) subtropical soils with some identified in temperate areas with (Turner et al. 2001) some species colonizing burnt environments with their spores activated by heat (Webster & Weber 2007). Forms mycelium and macroconidia in some cases forming pink or orange masses of macroconidia (Webster & Weber 2007). LL2 Aspergillus 0.0 99 2/1 Y Y LL2 branches close to Aspergillus penicillioides with strong penicillioides support (figure 3). Most of the Aspergillus species are soil fungi (AF548066) or saprophytes but some are capable of causing decay in storage, disease in plants or invasive disease in humans and animals and very abundant in most environments and as conidia in the air (Webster & Weber 2007). Aspergillus sp. are also reported as a marine pathogen causing disease of corals (Kim et al. 2006). AT2-4 Penicillium 0.0 99 AF530541 Y Y Y AT2-4 is a close relative of Penicillium expansum (figure 3). expansum (López- (unc Penicillium is a highly ubiquitous fungi occurring on a range of (AB028137) García et al. om decaying material (Webster & Weber 2007) which generally 2003) mon grow as mycelium forming hyphae. Some Penicillium ) (marneffei) will grow as a fission yeast at higher temperatures (Webster & Weber 2007). Penicillium expansum causes brown rot of apples (Webster & Weber 2007). p14A7 Penicillium 0.0 100 AY882533 Y Y Y Branches close to identified species (figure 3). 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