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A ne-scale spatial analysis of fungal communities on
tropical tree bark unveils the epiphytic rhizosphere in
orchids
Remi Petrolli, Conrado Augusto Vieira, Marcin Jakalski, Melissa F Bocayuva,
Clément Vallé, Everaldo da Silva Cruz, Marc-andré Selosse, Florent Martos,
Maria Catarina M. Kasuya
To cite this version:
Remi Petrolli, Conrado Augusto Vieira, Marcin Jakalski, Melissa F Bocayuva, Clément Vallé, et al.. A
ne-scale spatial analysis of fungal communities on tropical tree bark unveils the epiphytic rhizosphere
in orchids. New Phytologist, Wiley, In press, �10.1111/nph.17459�. �hal-03279090�
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A fine-scale spatial analysis of fungal communities on tropical tree bark unveils the
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epiphytic rhizosphere in orchids
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REMI PETROLLI
1*
, CONRADO AUGUSTO VIEIRA
1,2*
, MARCIN JAKALSKI
3
, MELISSA
4
F. BOCAYUVA
2
, CLEMENT VALLE
1
, EVERALDO DA SILVA CRUZ
2
, MARC-ANDRÉ
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SELOSSE
1,2,3
§
, FLORENT MARTOS
1
§
, MARIA CATARINA M. KASUYA
2
§
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1
Institut de Systématique, Évolution, Biodiversité (ISYEB), Muséum national d’Histoire
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naturelle, CNRS, Sorbonne Université, EPHE, CP 39, 57 rue Cuvier, F-75005 Paris, France
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2
Department of Microbiology, Viçosa Federal University (UFV), P. H. Rolfs street CEP:
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36570-900, Viçosa, Minas Gerais, Brazil
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3
University of Gdańsk, Faculty of Biology, ul. Wita Stwosza 59, 80-308 Gdańsk, Poland
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*
These authors contributed equally to this work.
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§
These authors supervised equally this work.
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Rémi Petrolli (Corresponding author)
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Muséum National d’Histoire Naturelle
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UMR 7205, Institut de Systématique, Évolution et Biodiversité (ISYEB),
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12 rue Buffon, CP 39, 75005 Paris, France
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Email : remi.petrolli@mnhn.fr
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6162 words: 842 words (Introduction), 1916 words (M&M), 1146 words (Results) and 2258
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words (Discussion). 5 colored figures, 1 table, and 23 supplementary figures and tables.
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We declare no conflict of interest regarding this work.
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Abstract
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• Approximately 10% of vascular plants are epiphytes and, even though this has long
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been ignored in past research, can interact with a variety of fungi, including mycorrhizal
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ones. However, the structure of fungal communities on bark, as well as their relationship
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with epiphytic plants, is largely unknown.
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• To fill this gap, we conducted environmental metabarcoding of ITS-2 region to
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understand the spatial structure of fungal communities of the bark of tropical trees, with
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a focus on epiphytic orchid mycorrhizal fungi, and tested the influence of root
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proximity.
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• For all guilds, including orchid mycorrhizal fungi, fungal communities were more
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similar when spatially closed on bark, i.e., displayed positive spatial autocorrelation.
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They also showed distance decay of similarity from epiphytic roots, meaning that their
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composition on bark increasingly differed, compared to roots, with distance from roots.
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• We first showed that all the investigated fungal guilds presented a spatial structure at
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very small scales. This spatial structure was influenced by the roots of epiphytic plants,
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suggesting the existence of an epiphytic rhizosphere. Finally, we showed that orchid
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mycorrhizal fungi were aggregated around them, possibly resulting from a reciprocal
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influence between the mycorrhizal partners.
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Key words
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epiphytism; fungal guilds; metabarcoding; fungal spatial distribution; orchid mycorrhizal fungi;
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Tulasnellaceae
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1. Introduction
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Although globally distributed, microorganisms present a highly variable local richness and a
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spatial structure at every scale (from centimeters to thousands of kilometers), especially in soils
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(Green et al., 2004; Green & Bohannan, 2006). Much of the soil microbial biodiversity appears
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to be intrinsically linked with plants in the rhizosphere and controls their community structure
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by monitoring soil-root interactions (Bever et al., 2010). Reciprocally, soil microorganisms that
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develop nutritional and protective symbioses with roots are especially structured by host
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presence and diversity (Peay et al., 2013) such as the mycorrhizal fungi that associate with
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approximately 90% of the vascular land flora (Van Der Heijden et al., 2015; Brundrett &
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Tedersoo, 2018). Fungal metabarcoding studies in soils have shown that the mycorrhizal taxa
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are not randomly distributed, but exhibit spatial structure at rather fine scales, in temperate as
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in tropical systems (Anderson et al., 2014; Bahram et al., 2016; Coince et al., 2013; Pickles et
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al., 2010; Tedersoo et al., 2010; Zhang et al., 2017), i.e., a patchiness due to host distribution,
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but also other factors such as spore dispersal and community interactions (Hanson et al., 2012).
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However, the characterization of the underground distribution of soil fungi (mycorrhizal fungi,
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saprotrophs or pathogens) is complicated by the three-dimensional nature of soils, since
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differences may exist between soil horizons (Anderson et al., 2014; Bahram et al., 2015).
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Unlike soils, tree barks can be easily investigated as their multiple layers can be sampled and
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sequenced at once, especially on young trees where the bark is usually thin. Thus, young barks
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can be seen as virtually two-dimensional and are ideal systems for surveying the spatial
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distribution of fungal communities and mycorrhizal taxa around their epiphytic plant hosts.
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Indeed, ca. 10% of vascular plant species root on barks in the tropical wet forests around the
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globe (Zotz, 2016). These plants have long been considered as essentially non-mycorrhizal in
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such aerial substrates (Lehnert et al., 2017; Brundrett & Tedersoo, 2018; but see Rowe &
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Pringle, 2005) and their fungal partners have thus so far largely been ignored. However, there
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is now growing interest in the field of epiphytic fungal endophytes which could strongly
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influence the dynamics of epiphyte plant populations (Leroy et al., 2019). One symbiosis that
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regularly occurs in the epiphytic habitats is the orchid mycorrhiza (Martos et al., 2012; Herrera
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et al., 2018; Novotná et al., 2018). Epiphytic orchids, representing no less than 80% of this
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hyper-diverse plant family (with over 25 000 species (Givnish et al., 2015)), harbor typical
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hyphal coils within their root cortical cells, which are formed by the same families but different
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species of saprotrophic basidiomycetes (Dearnaley et al., 2012; Martos et al., 2012; Xing et al.,
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2019) compared to soil. The fungi are also required for germination of the minute, nutrient-
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poor orchid seeds (Smith & Read, 2008). It was therefore hypothesized that the distribution of
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orchids must be constrained by that of their mycorrhizal fungi (McCormick & Jacquemyn,
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2014; McCormick et al., 2018)
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The distribution of orchid mycorrhizal fungi (OMF) has been investigated in soils (Jacquemyn
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et al., 2014, 2017; McCormick & Jacquemyn, 2014; McCormick et al., 2016, 2018; Voyron et
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al., 2017), but only marginally on barks (Kartzinel et al., 2013), perhaps because most studies
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focus on temperate and Mediterranean ecosystems where orchids are strictly terrestrial. For
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example, two recent studies (Waud et al., 2016b,a) showed a decline in abundance and
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similarity composition of OMF with distance from adult orchids, which likely explains the
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patchy distribution of grassland orchids (Jacquemyn et al., 2007, 2014). Still in grassland
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habitats, Voyron et al., (2017) found that communities of OMF are more similar in nearby soil,
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i.e., display spatial autocorrelation (Hanson et al., 2012). As for the epiphytic environment,
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very little is known on the spatial distribution of mycorrhizal fungi on bark [but see (Izuddin et
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al., 2019) for a first approach]. Similarly, the evolution of their community structure by distance
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