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Yeast forms dominate fungal diversity in the deep.rtf

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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                             10m 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). Penicillium is a
           namyslowskii                   (Stoeck et al.       (unc       highly ubiquitous fungi occurring on a range of decaying
           (AB028190)                     2006)                om         material (Webster & Weber 2007) which generally grow as
H48b       and       Eladia   0.0   99    AY256241             mon        mycelium forming hyphae. Some Penicillium (marneffei) will
           saccula                        (Stoeck et al.       )          grow as a fission yeast at higher temperatures (Webster &
           (AB031391)                     2003)                           Weber    2007).   Eladia   are   widespread    mitosporic   fungi
p15C07                        0.0   98    AY882538                        (Hawksworth et al. 1995)
                                          (Stoeck et al.
                                          2006)
DH148-5-                      0.0   98    AF290082
EKD21                                     (López-
                                          García et al.
                                          2001)
A1_E044                       0.0   98    AY046710
                                          (Edgcomb et
                                          al. 2002)
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