Leaf-associated fungal diversity in acidified streams:
insights from combining traditional and
molecular approaches
Hugues Clivot,
1,2
* Julien Cornut,
1,2,3,4
Eric Chauvet,
3,4
Arnaud Elger,
3,4
Pascal Poupin,
1,2
François Guérold
1,2
and Christophe Pagnout
1,2
1
Laboratoire Interdisciplinaire des Environnements
Continentaux (LIEC), Université de Lorraine, UMR
7360, Campus Bridoux rue du Général Delestraint,
57070 Metz, France.
2
LIEC, CNRS, UMR 7360, 57070 Metz, France.
3
Laboratoire d’Ecologie Fonctionnelle et Environnement
(EcoLab), INP, UPS, Université de Toulouse, UMR
5245, 118 Route de Narbonne, 31062 Toulouse,
France.
4
EcoLab, CNRS, UMR 5245, 31062 Toulouse, France.
Summary
We combined microscopic and molecular methods to
investigate fungal assemblages on alder leaf litter
exposed in the benthic and hyporheic zones of five
streams across a gradient of increasing acidification
for 4 weeks. The results showed that acidification
and elevated Al concentrations strongly depressed
sporulating aquatic hyphomycetes diversity in both
zones of streams, while fungal diversity assessed
by denaturing gradient gel electrophoresis (DGGE)
appeared unaffected. Clone library analyses revealed
that fungal communities on leaves were dominated by
members of Ascomycetes and to a lesser extent by
Basidiomycetes and Chytridiomycetes. An important
contribution of terrestrial fungi was observed in both
zones of the most acidified stream and in the
hyporheic zone of the reference circumneutral stream.
The highest leaf breakdown rate was observed in the
circumneutral stream and occurred in the presence of
both the highest diversity of sporulating aquatic
hyphomycetes and the highest contribution to clone
libraries of sequences affiliated with aquatic hypho-
mycetes. Both methods underline the major role
played by aquatic hyphomycetes in leaf decom-
position process. Our findings also bring out new
highlights on the identity of leaf-associated fungal
communities and their responses to anthropogenic
alteration of running water ecosystems.
Introduction
Fungi play a crucial role in detritus-based lotic ecosys-
tems as main microbial mediators of allochthonous leaf
litter decomposition (Findlay and Arsuffi, 1989; Baldy
et al., 1995; Gulis and Suberkropp, 2003). Aquatic fungi,
through their leaf-degrading enzyme capabilities, contrib-
ute to microbial leaf processing and improve the nutri-
tional quality of leaf litter for further consumption by
invertebrate detritivores (Bärlocher and Kendrick, 1981;
Arsuffi and Suberkropp, 1988). Aquatic hyphomycetes, a
polyphyletic group of fungi, are thought to dominate
microbial communities growing on decaying leaves
(Bärlocher, 1992; Suberkropp, 1992; Gessner et al.,
2007).
Both leaf litter breakdown and associated aquatic
hyphomycete diversity have been considered as useful
indicators of the functional integrity of streams (Gessner
and Chauvet, 2002) and as potential bioindicators of
anthropogenic stress (Solé et al., 2008). In particular,
reduced leaf litter breakdown and concurrent loss of
aquatic hyphomycete diversity have been reported in
numerous studies, notably under high concentrations of
metals such as Al in acidified streams (Baudoin et al.,
2008), Cd (Moreirinha et al., 2011), Ag (Pradhan et al.,
2011), Zn (Fernandes et al., 2009; Niyogi et al., 2009) or
even in the context of multiple (i.e. Cu and Zn) contami-
nants (Duarte et al., 2008). These observed decreases in
species richness under anthropogenic stress have tradi-
tionally been assessed using microscopic methods based
on the morphological identification of conidia (asexual
spores), which varies between species.
Recently developed molecular methods allow investi-
gation of fungal communities regardless of their life
history stage, including mycelia, which constitute the
metabolically active part of fungal biomass on leaves
(Bärlocher, 2007; 2010; Krauss et al., 2011). Molecular
fingerprinting of microbial communities, namely terminal
restriction fragment length polymorphism analysis and
denaturing gradient gel electrophoresis (DGGE), first
showed that the traditional method (conidial identification)
Received 14 May, 2013; revised 31 July, 2013; accepted 3 August,
2013. *For correspondence. E-mail hugues.clivot@univ-lorraine.fr;
Tel. (+33) 387378657; Fax (+33) 387378512.
Environmental Microbiology (2014) 16(7), 2145–2156 doi:10.1111/1462-2920.12245
© 2013 Society for Applied Microbiology and John Wiley & Sons Ltd