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Mycobiology Research Article Mycobiology Research Article Unique Phylogenetic Lineage Found in the Fusarium-like Clade after Re-examining BCCM/ IHEM Fungal Culture Collection Material David Triest1,*, Koen De Cremer2, Denis Piérard3 and Marijke Hendrickx1 1 BCCM/IHEM Collection of Biomedical Fungi, Service of Mycology & Aerobiology, Scientific Institute of Public Health, 1050 Brussels, Belgium 2 Service of Health & Environment, Scientific Institute of Public Health, 1050 Brussels, Belgium 3 Department of Microbiology & Infection Control, Universitair Ziekenhuis Brussel, Vrije Universiteit Brussel, 1090 Brussels, Belgium Abstract Recently, the Fusarium genus has been narrowed based upon phylogenetic analyses and a Fusarium-like clade was adopted. The few species of the Fusarium-like clade were moved to new, re-installed or existing genera or provisionally retained as “Fusarium.” Only a limited number of reference strains and DNA marker sequences are available for this clade and not much is known about its actual species diversity. Here, we report six strains, preserved by the Belgian fungal culture collection BCCM/ IHEM as a Fusarium species, that belong to the Fusarium-like clade. They showed a slow growth and produced pionnotes, typical morphological characteristics of many Fusarium-like species. Multilocus sequencing with comparative sequence analyses in GenBank and phylogenetic analyses, using reference sequences of type material, confirmed that they were indeed member of the Fusarium-like clade. One strain was identified as “Fusarium” ciliatum whereas another strain was identified as Fusicolla merismoides. The four remaining strains were shown to represent a unique phylogenetic lineage in the Fusarium-like clade and were also found morphologically distinct from other members of the Fusarium-like clade. Based upon phylogenetic considerations, a new genus, Pseudofusicolla gen. nov., and a new species, Pseudofusicolla belgica sp. nov., were installed for this lineage. A formal description is provided in this study. Additional sampling will be required to gather isolates other than the historical strains presented in the present study as well as to further reveal the actual species diversity in the Fusarium-like clade. Keywords Fusarium, Fusicolla, Microcera, Nectriaceae, Phylogeny, Pseudofusicolla In 2011, a phylogenetic study from Gräfenhan et al. [1] Fusarium clade.” In order to retain the monophyly of showed that the Fusarium genus (Hypocreales, Nectriaceae) Fusarium, Gräfenhan et al. [1] narrowed the generic concept was not monophyletic. They found that the genus was divided of Fusarium and the basal Fusarium clade was no longer into two groups in their phylogenic tree of Nectriaceae, considered as Fusarium sensu stricto. The few species and separated by a large number of species classified in genera lineages represented in this Fusarium-like clade were moved such as Neonectria and Volutella [1]. These groups were to new, re-installed or existing genera (i.e., Atractium, referred to as the “basal Fusarium clade” and the “terminal Microcera, Macroconia, Fusicolla, Dialonectria, and Stylonectria), or provisionally retained as “Fusarium” or as one of its teleomorphs (i.e., Nectria and Cosmospora), based upon Mycobiology 2016 September, 44(3): 121-130 phylogenetic and morphological analyses [1, 2]. http://dx.doi.org/10.5941/MYCO.2016.44.3.121 Recently, Lombard et al. [3] phylogenetically re-evaluated pISSN 1229-8093 • eISSN 2092-9323 © The Korean Society of Mycology the generic concepts in the Nectriaceae and confirmed the monophyly of each of these Fusarium-like genera. Lombard *Corresponding author E-mail: [email protected] et al. [3] also further narrowed Fusarium sensu Gräfenhan et al. [1] according to its internal phylogenetic structure Received March 29, 2016 Revised June 7, 2016 and thereby applied the “one fungus, one name” concept Accepted July 12, 2016 adopted in the International Code of Nomenclature for Algae, Fungi and Plants as of January 2013 in order to abolish This is an Open Access article distributed under the terms of the the dual naming system (cfr. teleomorphic name is preferred). Creative Commons Attribution Non-Commercial License (http:// They installed a new genus Bisifusarium and applied several creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, teleomorphic names for some important groups of Fusarium provided the original work is properly cited. anamorphs. In doing so, Lombard et al. [3] rejected the 121 122 Triest et al. “Fusarium-first” proposal made by the Fusarium working fragments of carnation leaf, at 23oC for 30 days under community [2] to conserve the name Fusarium above all alternating cycles of light (i.e., day) and dark (i.e., night) linked teleomorphic names for the sake of nomenclatural conditions. Growth rates were measured from the PDA stability as well as rejected their broad phylogenetic definition plates. Colony morphology, pigmentation, conidiogenesis, of Fusarium, which was based upon Fusarium sensu conidial characteristics, and presence of chlamydospores or Gräfenhan et al. [1] and the refinements made by O’Donnell other features were described from both the PDA and SNA et al. [4]. plates. Conidial measurements were taken from 20 randomly Species of the Fusarium-like clade are mostly slow growing selected conidia. A Nikon eclipse E600 microscope (Nikon, and produce a characteristic orange, conidial slime, known Tokyo, Japan) was used and pictures were recorded with as pionnotes, rather than an aerial mycelium [1]. Species the NIS-Elements BR 4.0 imaging software. The strains identification based upon morphology is difficult in the were described according to the terminology applied in Fusarium-like clade. They often occur as saprophytes in the “The Fusarium laboratory manual” of Leslie et al. [8]. soil, on trees or other fungi, and in aquatic environments [1, 2]. In contrast to the well-studied species diversity of Re-identification by multilocus sequencing. Multilocus Fusarium sensu Gräfenhan et al. [1], they have not been sequencing was applied on the six strains and comparative reported as plant pathogens or opportunistic human sequence analyses were performed in GenBank. The internal pathogens and only a few have been described to produce transcribed spacer (ITS) region and part of the ribosomal mycotoxins [2, 5]. Members of the Fusarium-like clade large subunit (LSU) were amplified as well as partial have therefore been largely neglected for a long period of fragments of the commonly used Fusarium DNA marker time. As a consequence, not much is known about the genes: translation elongation factor 1-alpha (TEF1α), beta- actual phylogenetic species diversity in this clade. It was tubulin (BT), and the second largest subunit of RNA only after the taxonomical revision of Gräfenhan et al. [1] polymerase II (RPB2). DNA extraction, PCR amplification, that some DNA marker sequences became available. and sequencing were achieved according to the protocol Among the Fusarium strains preserved by the Belgian applied by Beguin et al. [9]. Primers were described previously: culture collection of biomedical fungi BCCM/IHEM, six for ITS by White et al. [10], for LSU by Hopple and appeared to belong to the Fusarium-like clade based upon Vilgalys [11], for TEF1α by Carbone and Kohn [12], for their morphological appearance during re-identification [6]. BT by Glass and Donaldson [13], and for RPB2 by Van All six strains were slow growing and produced pionnotes, Hove et al. [14]. i.e., typical morphological characteristics of only some Fusarium, but many Fusarium-like species. The objective Phylogenetic analyses. In order to determine whether of the present study was to determine whether these strains our six strains belong to the Fusarium-like clade in the indeed belong to the Fusarium-like clade in the phylogeny phylogeny of the Nectriaceae, a Bayesian phylogenetic analysis of the Nectriaceae as well as to confirm their identity up to was conducted. Therefore, we used the ITS and RPB2 the genus and species level. This was achieved by performing reference sequences of type material published by Gräfenhan multilocus sequencing and phylogenetic analyses using et al. [1] and included our strains. The combined sequence reference sequences of type material. Also morphological dataset was first aligned by the ClustalW algorithm in analyses and mating experiments were performed. MEGA4 [15] and edited manually. Four ambiguously aligned regions (two in the ITS and two in the RPB2 gene marker) MATERIALS AND METHODS were excluded from the analysis. Subsequently, Bayesian inference analysis was executed with MrBayes3.2 [16], Strains. The six strains, used in this study, were collected applying the GTR + I + Γ model of evolution for both loci and preserved by the BCCM/IHEM fungal culture collection and estimating parameters separately for each locus. The after their isolation from different substrates (Table 1). All Monte Carlo Markov chain method was used with runs of were identified based upon their morphology and identified one million generations and sampling a tree every 100 as a Fusarium species at the time of their deposit in the generations. The first 25% of sampled trees were discarded collection, more than 20 years ago. They were recently (i.e., burn-in) and the consensus tree, with posterior subjected to re-identification, together with the other probabilities, was assessed from the remaining trees. The Fusarium strains in the BCCM/IHEM
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