Lechat C. & Fournier J. Varicosporella, a new aquatic genus in the Nectriaceae from France. 2015. Ascomycete.org. 7(1): 1-8

Abstract

Varicosporella aquatica gen. and sp. nov. is described and illustrated based on six collections on submerged wood in South of France. A fusarium-like asexual morph was obtained in culture and sequenced. The genus is placed in the Nectriaceae based on its asexual morph and phylogenetic comparison of ITS and LSU sequences with species in 22 genera of Hypocreales including 16 genera in the Nectriaceae. It is primarily characterized by obpyriform, greyish yellow to pale orange nonstromatic ascomata, short-ribbed ascospores and freshwater habitat.

Full text

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Varicosporella, a new aquatic genus in the Nectriaceae
from France
Christian LECHAT
Jacques FOURNIER
Ascomycete.org, 7 (1) : 1-8.
Février 2015
Mise en ligne le 12/02/2015
Summary: Varicosporella aquatica gen. and sp. nov. is described and illustrated based on six collections on
submerged wood in South of France. A fusarium-like asexual morph was obtained in culture and sequenced.
The genus is placed in the Nectriaceae based on its asexual morph and phylogenetic comparison of ITS and
LSU sequences with species in 22 genera of Hypocreales including 16 genera in the Nectriaceae. It is primarily
characterized by obpyriform, greyish yellow to pale orange nonstromatic ascomata, short-ribbed ascospores
and freshwater habitat.
Keywords: Ascomycota, freshwater habitat, Hypocreales, ribosomal DNA, taxonomy.
Résumé : Varicosporella aquatica gen. et sp. nov. est décrite et illustrée d’après six récoltes, sur bois immergé,
eectuées dans le sud de la France. Un stade asexué de type fusarium a été obtenu en culture et séquencé.
Le placement du nouveau genre dans les Nectriacées repose sur le stade asexué et sur la comparaison phy-
logénétique de ses séquences ITS et LSU avec celles de 22 genres d’Hypocréales incluant 16 genres de Nec-
triacées. Il est principalement caractérisé par des ascomes obpiriformes, non stromatiques, de couleur jaune
grisâtre à orange pâle, des ascospores ornées de courtes crêtes leur donnant un aspect variqueux et un ha-
bitat aquatique.
Mots-clés : Ascomycota, habitat aquatique, Hypocréales, ADN ribosomal, taxinomie.
Introduction
In the course of an ongoing survey of freshwater pyrenomycetes
in southwestern France several hypocrealean fungi have been re-
peatedly collected, which proved dierent from known terrestrial
species and dierent from species reported in the literature and lis-
ted at http://fungi.life.uiuc.edu/world_records (SHEARER & RAJA, 2010).
One of them, Lasionectria fournieri Lechat (LECHAT, 2008), was descri-
bed as new but most of them are still under investigation. These
fungi frequently occur in very small colonies and their isolation
often proves unsuccessful, rendering their characterization unsatis-
fying. Aquatic hypocrealean fungi are poorly represented in the li-
terature, usually reported under the genus name Nectria (Fr.) Fr. in a
very broad sense. Often only limited information on morphological
data accompanies the records, which rarely allows a generic place-
ment, let alone species delimitation. Moreover the available infor-
mation often suggests that terrestrial fungi fortuitously present in
water are more likely involved rather than true aquatic fungi. It is
noteworthy that the aquatic hypocrealean fungi we encountered
appear erumpent from the wood and gradually become almost su-
percial with the base remaining slightly immersed and are never
stromatic. These features, especially the erumpent habit, are usually
not encountered in terrestrial species and might relate to their aqua-
tic lifestyle.
A distinctive taxon characterized by obpyriform greyish yellow to
pale orange ascomata and pale yellow brown ascospores with
short-ribbed ornamentation was repeatedly collected on submer-
ged wood; the ascomata did not change colour in KOH. This species
may be accommodated in the Bionectriaceae (ROSSMAN et al., 1999).
Unexpectedly, its ascomatal wall appeared to turn pale yellow in
lactic acid, suggesting possible anities with the Nectriaceae, which
was conrmed by a fusarium-like asexual morph obtained in arti-
cial culture, which is unknown in the Bionectriaceae. Further mole-
cular analyses of ITS and LSU sequences compared with those of 22
genera of Hypocreales including 16 genera in the Nectriaceae and
six in the Bionectriaceae (Table 1) supported its placement in the
Nectriaceae, in a clade composed of morphologically unrelated ter-
restrial taxa.
For these reasons we conclude that this fungus represents a pre-
viously undescribed genus in the Nectriaceae and we propose the
new genus Varicosporella to accommodate the new species Varicos-
porella aquatica.
Materials and Methods
Specimens were examined using the method described by ROSS-
MAN et al. (1999). Microscopic observations and measurements were
made in water. The ascospore ornamentation was observed in lactic
Cotton Blue not heated. The holotype specimen and paratypes are
deposited in LIP herbarium (University of Lille) and cultures at CBS.
Cultures of the living specimen were made on PDA (Potato Dextrose
Agar) with 5 mg/l of streptomycin in Petri dishes 9 cm diam. A mass
of ascospores and asci was removed from a perithecium with a ne
needle and placed in a drop of sterile water that was stirred with a
needle to distribute the elements on the slide. A part of the drop
containing ascospores was placed on PDA using a sterile micropi-
pette, then the Petri dish was incubated at 25°C.
DNA extraction, amplication, and sequencing were performed
by ALVALAB (Santander, Spain): Total DNA was extracted from dry
specimens blending a portion of them using a micropestle in 600 μL
CTAB buer (CTAB 2%, NaCl 1.4 M, EDTA pH 8.0 20 mM, Tris-HCl pH
8.0 100 mM). The resulting mixture was incubated for 15 min. at
65ºC. A similar volume of chloroform: isoamylalcohol (24:1) was
added and carefully mixed with the samples until their emulsion.
It was then centrifuged for 10 min at 13.000 g, and the DNA in the
supernatant was precipitated with a volume of isopropanol. After a
new centrifugation of 15 min at the same speed, the pellet was wa-
shed in cold ethanol 70%, centrifuged again for 2 min and dried. It
was nally resuspended in 200 μL ddH2O. PCR amplication was
performed with the primers ITS1F and ITS4 (WHITE et al., 1990; GARDES
& BRUNS, 1993) for ITS, while LR0R and LR5 (VILGALYS & HESTER, 1990)
were used to amplify the 28S nLSU region. PCR reactions were per-
formed under a program consisting of a hot start at 95ºC for 5 min,
followed by 35 cycles at 94ºC, 54ºC and 72ºC (45, 30 and 45 s res-
pectively) and a nal 72ºC step 10 min. PCR products were checked
in 1% agarose gels, and positive reactions were sequenced with pri-
mer ITS4. Chromatograms were checked searching for putative rea-
ding errors, and these were corrected.
Analyses were performed online at www.phylogeny.lirmm.fr (DE-
REEPER et al., 2008). Maximum likelihood phylogenetic analyses were
performed with PhyML 3.0 aLRT (ZWICKL, 2006), using the GTR + I +
Γ model of evolution. Branch support was assessed using the non-
parametric version of the approximate likelihood-ratio test, imple-
mented in PhyML (SH-aLRT; ANISIMOVA & GASCUEL, 2006).

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Taxonomy
Varicosporella Lechat & J. Fourn. gen. nov. — MB 810690
Diagnosis: Diers from other genera of the Nectriaceae with fu-
sarium-like asexual morph by pale orange nonstromatic ascomata
not changing colour in KOH, aquatic habitat and ascospores conspi-
cuously ornamented with short sinuous ribs.
Type species: Varicosporella aquatica Lechat & J. Fourn.
Etymology: “Varicosporella” refers to the ribbed ornamentation
of ascospores, from Latin varix = varicose vein.
Varicosporella aquatica Lechat & J. Fourn. sp. nov. — MB 810691,
Plates 1-2.
Diagnosis: Ascomata on submerged wood, supercial, nonstro-
matic, obpyriform, pale orange, not turning red or purple in 3% KOH,
turning pale yellow in lactic acid, wall 28–35 μm thick composed of
thick-walled angular to attened cells; hamathecium of fugacious
moniliform paraphyses, asci 8-spored, cylindric-clavate with a J- at-
tened apical apparatus; ascospores 21–24 × 8.5–10 μm, equally two-
celled, pale yellow brown, ornamented with short sinuous ribs.
Holotype: France, Ariège, Vernajoul, Vernajoul brook, ca. 350 m
asl, on submerged wood of Populus sp., associated with Bactrodes-
mium obovatum and Cosmospora sp., 6 Jul. 2009, JF 09197 (LIP). Ex-
type culture CBS126103, ITS and LSU GenBank sequences KP192669
and KP192671.
Etymology: The epithet refers to the freshwater lifestyle of the
fungus.
Known distribution: South of France: Ariège, Lozère.
Ascomata nonstromatic, solitary, supercial with base slightly im-
mersed in substratum, soft-textured, greyish yellow to pale orange,
becoming pale yellow in 3% KOH and in lactic acid, obpyriform,
340–390 μm high × 250–300 μm diam. (Me = 370 × 285 μm, n = 10),
laterally collapsing when dry, uniloculate, translucent, with a broadly
conical to rounded apex 100–170 μm long, 80–110 μm diam, com-
posed of cylindrical yellow cells 15–40 μm long, 3.5–4.5 μm diam,
thick-walled, septate, clavate at top.
Ascomatal wall in vertical section 28–35 μm thick, composed of
subglobose to angular thick-walled cells, wall 1.5–2.5 μm thick, be-
coming more attened inwardly. Perithecial surface cells forming a
textura angularis in surface view. Basal hyphae sparse and short,
thick-walled, hyaline. Asci unitunicate, cylindrical, short–stipitate,
with eight obliquely uniseriate ascospores, 140–165 × 17–20 μm,
apically truncate to slightly rounded with a conspicuous, refractive
apical apparatus 1.5–2 μm high × 5–6 μm wide, discoid to wedge-
shaped, slightly stained in blue ink, interspersed with slightly mo-
niliform, thin-walled, early deliquescing paraphyses 8–14 μm wide
at base. Periphyses copious, embedded in gel matrix, simple or
branched, septate, 15–40 × 1.5–2 μm. Ascospores 21–24 × 8.5–10
(–11) μm (Me = 22.5 × 9.5 μm, n = 30), ellipsoid with narrowly to
broadly rounded ends, equally two-celled, slightly constricted at
septum, hyaline to pale yellowish brown, with two large guttules in
each cell, wall roughened by short, sinuous, brown, thick ribs, so-
metimes anastomosed. Hyaline ascospores germinate more often
than pigmented ones.
Cultural characteristics: After 20 days at 25°C on Difco PDA
containing 5 mg/L streptomycin, colony 3.5–4 cm diam., producing
fast-growing fusarium-like, culture slimy, lacking aerial mycelium,
white to pale yellowish, becoming pale pinkish and cottony with
aerial mycelium. No microconidia produced; macroconidia cylindri-
cal, slightly curved, acute at tip, truncate to rounded at base, 3–4
(–5)-septate: 3-septate (62–) 67–75 (–78) × 7–8.5 μm (Me = 72 ×
8 μm, n = 30), 4–5-septate (72–) 75–77 (–85) × 7–8.5 μm (Me = 77.4
× 8 μm, n = 30). Pale yellow fertile ascomata produced on cultures
after ve weeks, containing asci and ascospores identical to the
type.
Additional specimens examined: FRANCE: Ariège, Clermont, Le
Pujol brook along road D 119, ca. 360 m asl, on submerged twig of
Buxus sempervirens, 31 Jul. 2009, JF 09213 (LIP), (Cultured,
CBS125538); Ariège, Vernajoul, Vernajoul brook, Pont Fagé, ca. 370
m asl, on submerged wood of Salix sp., soc. Jahnula aquatica, Lenti-
thecium aquaticum and Pseudohalonectria lutea, 18 Jul. 2013,
JF13150 (LIP); Ariège, Vernajoul, Vernajoul brook, Pont Fagé, on sub-
merged wood of Alnus glutinosa, soc. Jahnula aquatica, Pseudoha-
lonectria lutea, 18 Jul. 2013, JF13152 (LIP); Ariège, Castelnau-Durban,
L’Artillac, on submerged wood of Fraxinus soc. Jahnula aquatica,
Lindgomyces griseosporus, Pleurotheciella rivularia and Trematos-
phaeria hydrela, 24 Jul. 2014, JF14074 (LIP), (Cultured, CBS138883,
ITS and LSU GenBank sequences KP192668 & KP192670); Lozère,
Saint-Germain-du-Teil, Malbousquet brook, 3°12’00’’ E, 44°28’03” N,
575 m asl, on submerged wood, 23 Oct. 2014, leg. A. Gardiennet,
pers. herb. AG14191.
Discussion
Varicosporella aquatica is characterized by supercial, nonstroma-
tic obpyriform ascomata with a soft pale orange peridium that does
not turn red or purple in 3% KOH, unitunicate cylindrical asci with a
discoid refractive inamyloid apical apparatus, deliquescent para-
physes and equally two-celled, pale brown ascospores ornamented
with short sinuous ridges; its asexual morph obtained in culture is
fusarium-like.
Based on the characters of its sexual and asexual morphs, this
taxon clearly belongs to the Hypocreales, either in the Bionectriaceae
or in the Nectriaceae as dened by ROSSMAN et al. (1999) and SCHROERS
(2001). The pale orange ascomata not changing color in 3% KOH or
lactic acid are typical of the Bionectriaceae but a fusarium-like
asexual morph is unknown in this family and is only represented in
the Nectriaceae. The delimitation of the two families is largely based
on the type of asexual morph and strongly supported by phyloge-
netic studies (ROSSMAN, 2000; ROSSMAN et al., 2013). Therefore, our new
taxon having a fusarium-like asexual morph is best placed in the
Nectriaceae, which is well supported by our phylogenetic analysis
(Fig. I).
Unlike Varicosporella, most genera of the Nectriaceae typically
have dark orange to red ascomata that turn darker red or purple in
KOH, and yellow in lactic acid (ROSSMAN et al., 1999). However two
genera currently accommodated in the Nectriaceae likewise lack the
typical KOH reaction, viz. Albonectria Rossman & Samuels and Pseu-
donectria Seaver (ROSSMAN et al., 1999). Albonectria diers from Vari-
cosporella in having warted, thick-walled, white ascomata on a
sparse to well-developed pseudoparenchymatous stroma and 3-to
multiseptate ascospores, while Pseudonectria has thin-walled asco-
mata (wall less than 20 μm thick), usually nonseptate smooth
ascospores and a volutella-like asexual morph.
Molecular analysis carried out in the present study, comparing 16
genera in the Nectriaceae including the type species of Albonectria
and Pseudonectria (Fig. 1), shows that Varicosporella is nested within
the Nectriaceae but placed on a basal branch distant from other ge-
nera clustering in the same subclade, viz. Viridispora Samuels & Ross-
man, and Neocosmospora E.F. Sm.
Viridispora diers from Varicosporella in having red strongly war-
ted or roughened ascomata, penicillifer-like asexual morph and
green to yellow brown, smooth ascospores. Neocosmospora resem-
bles Varicosporella in having often pigmented and coarsely orna-
mented ascospores but is readily distinguished in having smooth
or roughened to coarsely warted, orange brown to red ascomata,
turning reddish brown to dark purple in 3% KOH.
Moreover, none of the genera discussed above was reported to
occur on submerged wood in freshwater habitats. The aquatic life-
style of V. aquatica is supported by six collections on submerged

3
wood, often associated with known aquatic ascomycetes (Plate 2,
Fig. a), and no occurrence on terrestrial substrates despite extensive
collecting and investigations on pyrenomycetes over the last 15
years in the same area (Ariège). A thorough comparison with the
descriptions of hypocrealean ascomycetes recorded in freshwater
habitats by SHEARER (1993), CAI et al. (2003), CAI et al. (2006) and SHEA-
RER & RAJA (2010) at http://fungi.life.uiuc.edu/world_records did not
show any genus or species conforming to the peculiar combination
of characters displayed by V. aquatica. Thus, based on morphologi-
cal, cultural, molecular and ecological data, a new nectriaceous
genus Varicosporella is introduced to accommodate V. aquatica.
The new rules imposed by the ICN at Melbourne Congress in 2011
(MCNEILL et al., 2012) specify that in pleomorphic fungi a new genus
name cannot be introduced when an older name is available for the
asexual or the sexual morph. Following these rules one might consi-
der the genus name Fusarium Link for our new taxon which has a
fusarium-like asexual morph. The status of Fusarium as a genus
name is controversial since its origin, having been split into various
“sections”. The genus in the broad sense was recently delimited into
“a” Fusarium terminal clade, distant from other “basal fusarium-like
clades” by GRÄFENHAN et al. (2011). The terminal clade proposed by
these authors includes the type species F. sambucinum Fuckel as its
sexual morph Gibberella pulicaris (Fr.) Sacc., along with sexual
morphs described in Albonectria, Cyanonectria, Haematonectria and
Neocosmospora, but “without signicant statistical support” (GRÄ-
FENHAN et al., 2011). On the one hand phytopathologists strongly ad-
vocate for Fusarium to represent the whole terminal clade (GEISER et
al., 2013) while on the other hand taxonomists reasonably assign
Fusarium to the monophyletic group of species clustering around
F. sambucinum (SCHROERS et al., 2011; ROSSMAN, 2013). Our new species
Fig. 1 — Maximum likelihood phylogeny of Varicosporella based on combined ITS1-5.8S-ITS2 and LSU sequences.

4
Plate 1. a–e: Varicosporella aquatica (Holotype JF09197). a: Perithecium on natural substratum. b: Close-up of perithecium in water. c:
Section through the ascomatal wall. d: Ascus and ascospores (in water). e: Close-up of ascospores in water showing ornamentation.

5
Plate 2. a–e: Varicosporella aquatica (Holotype JF09197). a: Perithecium on natural substratum mixed with Cosmospora sp. and Bactrodes-
mium obovatum. b: Germinating ascospores. c: Culture in Petri dish. d: Conidiophores and conidia. e: Conidia. f: Ascomata appearing after
ve weeks in culture.

6
Table 1 — Genera, species and GenBank accession numbers of sequences used in the phylogenetic analyses. The taxon names are from GenBank.
GenBank accession numbers
Species Asexual morph ITS LSU
Albonectria rigidiuscula (Berk. & Broome) Rossman & Samuels fusarium-like HM054158 HM042403
Bionectria ochroleuca (Schwein.) Schroers & Samuels clonostachys-like KF055399 GQ50600
Bionectria byssicola (Berk. & Broome) Schroers & Samuels clonostachys-like AF358252 GQ506011
Calonectria lauri (Vanderw.) Lechat & Crous cylindrocladium-like GQ280584 GQ280706
Cosmospora viliuscula (Samuels, Yoshim. Doi & Rogerson) Rossman & Samuels acremonium-like KC291732 KC291777
Cosmospora viridescens (C. Booth) Gräfenhan & Seifert acremonium-like KC291731 KC291765
Cyanonectria buxi (Fuckel) Schroers, Gräfenhan & Seifert fusarium-like HQ728144 HM626673
Gibberella pulicaris (Kunze) Sacc. fusarium-like KC445242 U85523
Gibberella zeae (Schwein.) Petch fusarium-like HQ651168 HQ147601
Hydropisphaera bambusicola Lechat acremonium-like GU059594 GU059595
Hypomyces armeniacus Tul. & C. Tul. cladobotryum-like FN859424 AF160239
Lanatonectria avolanata (Berk. & Broome) Samuels & Rossman actinostilbe-like EF121860 HQ232157
Lanatonectria occulenta (Henn. & E. Nyman) Samuels & Rossman actinostilbe-like JF832657 JF832714
Lasionectria mantuana (Sacc.) Cooke acremonium-like HM484858 GQ505994
Microcera larvarum (Fuckel) Gräfenhan, Seifert & Schroers fusarium-like KC354705 KC338992
Microcera coccophila Desm. fusarium-like KC338994 KC338993
Nalanthamala psidii (Sawada & Kuros.) Schroers & M.J. Wingf. nalanthamala-like AY554208 AY554255
Nectria cinnabarina (Tode : Fr.) Fr. tubercularia-like HM484712 HM484756

7
Table 1 — (continued)
GenBank accession numbers
Species Asexual morph ITS LSU
Nectria haematococca Berk. & Broome fusarium-like AY354252 AY489729
Nectria pseudotrichia (Schwein.) Berk. & M. A. Curtis tubercularia-like KF611683 JF832704
Nectriopsis sporangiicola (Samuels) Samuels acremonium-like AF210661 AF210662
Nectriopsis exigua (Pat.) W. Gams acremonium-like HM484865 GQ505986
Neocosmospora vasinfecta E.F. Sm. fusarium-like AY381155 AY381155
Neocosmospora ornamentata M.A.F. Barbosa fusarium-like AF178413 AF178382
Neonectria ditissima (Tul. & C. Tul.) Samuels & Rossman cylindrocarpon-like HM364298 HM364311
Pseudocosmospora eutypae C. Herrera & P. Chaverri acremonium-like KC291735 KC291766
Pseudocosmospora rogersonii C. Herrera & P. Chaverri acremonium-like KC291729 KC291780
Pseudonectria pachysandricola B.O. Dodge volutella-like JF832658 JF832715
Pseudonectria rousseliana (Mont.) Wollenw. volutella-like JF937565 JF937575
Roumegueriella rufula (Berk. & Broome) Malloch & Cain gliocladium-like -GQ505999
Rubrinectria olivacea (Seaver) Rossman & Samuels nalanthalama-like AY554219 AY554244
Selinia pulchra (G. Winter) P. Karst. acremonium-like HM484859 GQ505992
Viridispora diparietispora (J.H. Mill., Giddens & A.A. Foster) Samuels & Rossman penicillifer-like HM484859 AY489735
Varicosporella aquatica Lechat & J. Fourn. JF09197 fusarium-like KP192669 KP192671
Varicosporella aquatica Lechat & J. Fourn. JF14074 fusarium-like KP192668 KP192670

8
belongs to this “terminal clade” but is clearly distant from Fusarium
sensu Gibberella and stands apart on a basal branch.
Based on phylogenetic, morphological and ecological diver-
gences, our new taxon cannot be accommodated in any of the li-
neages given in GRÄFENHAN et al. (2011) nor in any known sexual
morph, thus we propose the new genus Varicosporella.
Acknowledgments
We gratefully acknowledge Dr. Amy Rossman (Systematic Myco-
logy & Microbiology Laboratory, USDA-ARS, Beltsville, USA) for her
constant support and her judicious improvements suggested to our
manuscript before submission. Dr. Pierre-Arthur Moreau (Labora-
toire des sciences végétales et fongiques, Faculté des sciences phar-
maceutiques et biologiques, Université de Lille 2, France) is warmly
thanked for his precious help to C. L. with phylogenetic analyses.
We likewise acknowledge Alain Gardiennet (Véronnes, France) for
his cheerful friendship and his ecient help with collecting aquatic
pyrenomycetes.
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Jacques Fournier
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jacques.fournier@club-internet.fr
Christian Lechat
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