1. Introduction
Bamboo fungi are a highly diverse group of organisms [1,2,3,4,5], and research on bambusicolous fungi also provides opportunities to control bamboo diseases and promote bamboo cultivation [6]. Approximately 150 basidiomycetes and 1150 ascomycetes have been reported from bamboo, including 350 asexual morphs, 240 hyphomycetes, and 110 coelomycetes [4,6]. China is rich in bamboo resources, and its bamboo species account for more than 50% of the world’s bamboo [7,8]. Sichuan Province has a variety of bamboo forests and inhabits a large number of bamboo fungi due to its complex topography and climate conditions [9]. Some well-represented families of bamboo fungi in Sichuan Province are Astrosphaeriellaceae [10], Bambusicolaceae [9,11], Occultibambusaceae [9,12] distributed in Dothideomycetes, and Apiosporaceae [12,13], Nectriaceae [10,14], Phyllachoraceae [10,15] distributed in Sordariomycetes.
Savoryellaceae (Savoryellales, Sordariomycetes), with an estimated divergence crown age of 182 MYA [16], contains generally saprobic fungi on bamboos, palms, Pandanus, Machilus sp., Pinus sp., or other unidentified woody substrates in terrestrial, freshwater, marine, brackish water, and water-cooling towers [16,17,18,19,20,21,22]. The family currently comprises six genera: Ascotaiwania, Bactrodesmium, Canalisporium, Dematiosporium, Neoascotaiwania, and Savoryella [17,23], which are characterized by immersed or superficial, globose to pyriform ascomata with paraphyses, two-to-eight-spored, clavate to cylindrical, unitunicate asci with an inamyloid apical ring, and ellipsoid, fusiform ascospores, with or without a gelatinous sheath, as well as a dematiaceous hyphomycetous asexual morph with globose to subglobose or obovate to oval conidia [24,25].
Members of Savoryellaceae are often found in freshwater habitats [17,23,26]. For example, the genus Canalisporium is found in freshwater habitats and typified by C. caribense [27]. Most Canalisporium species are characterized by dark brown and muriform conidia [27]; Canalisporium grenadoideum (=Ascothailandia grenadoidea) is the only species that represents a sexual morph: globose, dark brown, ostiolate ascomata, eight-spored, long cylindrical, unitunicate asci, fusiform, three-euseptate ascospores [28]. Dematiosporium, typified by D. aquaticum, and currently consist of species, in particular, from freshwater habitat [17,26]. This genus is characterized by cylindrical, unbranched, aseptate conidiophores and globose to subglobose, dictyospores conidia with a pore in each cell [17,26]. The generic type of Savoryella, S. lignicola, was initially discovered during a survey of cellulolytic fungi in a simulated aquatic environment and has been subsequently recovered from different woody substrates (i.e., Bambusa sp.) in aquatic or marine habitats [18,21,29]. Members of Savoryella are characterized by immersed, partly immersed, or superficial, globose, subglobose, or ellipsoidal ascostromata, two-to-eight-spored, cylindrical or clavate, unitunicate asci with an apical truncate non-amyloid apical thickening containing a pore and uni- or biseriate, ellipsoidal, three-septate ascospores [18,30]; as well as dematiaceous hyphomycetes, which produce micronematous conidiophores, holoblastic, terminal, and intercalary conidiogenous cells, solitary or aggregated, pyriform to obovoid, septate conidia [19].
During a survey of saprobic fungi from bamboo in Sichuan Province, China, a series of asexual and sexual fungi were collected. Multi-gene phylogeny integrated with morphological comparison was carried out to determine the taxonomic status of these new collections, of which new species and new host records contributed to Canalisporium, Dematiosporium, and Savoryella were introduced and justified to the Savoryellaceae.
2. Materials and Methods
2.1. Isolation and Morphological Examination
Fungi associated with decaying bamboo were collected from Dujiangyan and Qionglai in Sichuan Province, China in 2021. Specimens were placed in envelopes or plastic bags and taken to the laboratory. Morphological characteristics were observed using a Nikon ECLIPSE E200 stereo microscope and photographed by a Nikon ECLIPSE Ni-U compound microscope fitted with a Nikon DS-Ri2 digital camera as per the guidelines provided in Senanayake et al. [31]. Single-spore isolations were used to obtain pure cultures following the methods described by Senanayake et al. [31]. Measurements were made with the Tarosoft (R) Image Framework program v. 0.9.7, following Liu et al. [32]. Photo plates representing fungal structures were processed in Adobe Photoshop CS6 software (Adobe Systems Inc., San Jose, CA, USA). Herbarium specimens (dry branches with fungal material) were deposited in the herbarium of Cryptogams, Kunming Institute of Botany Academia Sinica (KUN-HKAS), Kunming, China and the herbarium of the University of Electronic Science and Technology (HUEST), Chengdu, China. The isolates obtained in this study were deposited in China General Microbiological Culture Collection Center (CGMCC) in Beijing, China and the University of Electronic Science and Technology Culture Collection (UESTCC) in Chengdu, China. Names of the new taxa were registered in MycoBank [33].
2.2. DNA Extraction, PCR Amplification and Sequencing
A Trelief TM Plant Genomic DNA Kit (Beijing TsingKe Biotech Co., Ltd., Beijing, China) was used to extract total genomic DNA from fungal mycelia. DNA amplification was performed by a polymerase chain reaction (PCR). Five partial gene regions, the small subunit of nuclear ribosomal RNA gene (SSU), the nuclear ribosomal internal transcribed spacer (ITS: ITS1-5.8S-ITS2), the large subunit of nuclear ribosomal RNA gene (LSU), the second-largest subunit of RNA polymerase II (rpb2), and the translation elongation factor 1-alpha (tef1α), were used in this study. Sequences of SSU, ITS, LSU, rpb2, and tef1α were amplified using primer pairs NS1/NS4, ITS5/ITS4, LR0R/LR5, fRPB2-5F/fRPB2-7cR, and 983F/2218R, respectively [34,35,36,37]. The amplification reactions were performed in 50 μL PCR mixtures containing 25 μL 2× Taq Plus MasterMix (Dye) (CoWin Biosciences, (Taizhou), Co., Ltd., Taizhou, China), 20 μL ddH2O, 1μL DNA template, and 2μL of each primer (10µM/L). The PCR thermal cycle program for SSU, ITS, LSU, rpb2, and tef1α amplification was as follows: initial denaturing step of 94 °C for 5 min, followed by 35 cycles of denaturation at 94 °C for 30 s, annealing at 56 °C (SSU, ITS, LSU, rpb2), 62 °C (tef1α) for 30 s, elongation at 72 °C for 30 s, and final extension at 72 °C for 5 min. PCR products were checked on 1% agarose electrophoresis gels stained with Gel Red. The sequencing reactions were carried out with primers mentioned above by Beijing Tsingke Biotechnology Co., Ltd., Chengdu, China.
2.3. Phylogenetic Analyses
The BLAST searches were performed for finding similar sequences that match our data. A concatenated dataset of the SSU, ITS, LSU, rpb2, and tef1α sequences were used for phylogenetic analyses with the inclusion of reference taxa from GenBank (Table 1). The sequences were aligned by using the online multiple alignment program MAFFT v.7 (
3. Results
3.1. Phylogenetic Analyses
To determine the phylogenetic placement of the new collections in this study, the combined SSU, ITS, LSU, rpb2, and tef1α data set comprised 55 sequences with Pleurotheciella aquatica (MFLUCC 17-0464) and P. erumpens (CBS 142447) as the outgroup taxa. The concatenated matrix comprised a total of 4870 characters (SSU: 1081 bp; ITS: 841 bp; LSU: 921 bp; rpb2: 1056 bp; tef1α: 971 bp) including gaps. Maximum likelihood (ML) and Bayesian inference (BI) analyses were resulting in generally congruent topologies. The best-scoring ML tree (Figure 1) was selected to represent the relationships among taxa, in which a final likelihood value of –37,950.559206 is presented. The evolutionary models for Bayesian analysis were selected for each locus, and the best-fit model GTR+I+G for ITS, LSU, rpb2, and tef1α, SYM+I+G for SSU, respectively. Six simultaneous Markov chains were run for 165,000 generations, and trees were sampled every 1000 generations and 165 trees were obtained. The first 33 trees representing the burn-in phase of the analyses were discarded, while the remaining 132 trees were used for calculating posterior probabilities in the majority rule consensus tree (critical value for the topological convergence diagnostic is 0.01).
Forty-three representative species of Savoryellaceae are included in our phylogenetic analysis (Figure 1). Two isolates of Canalisporium sichuanense (CGMCC 3.23926, UESTCC 22.0060) were sister to C. dehongense (MFLUCC 18-1396 and UESTCC 22.0056) and were well supported (100% ML/1.00 BYPP). Three isolates of Dematiosporium bambusicola (CGMCC 3.23774, UESTCC 22.0058, UESTCC 22.0059) formed a distinct clade sister to Dematiosporium aquaticum (CBS 144793, MFLU 18-1641, UESTCC 22.0055) with high statistical support (100% ML/1.00 BYPP). Two isolates of Savoryella bambusicola (CGMCC 3.23775 and UESTCC 22.0057) were nested in the genus Savoryella and close to S. lignicola (NF 00204).
3.2. Taxonomy
Canalisporium dehongense W. Dong, H. Zhang, and K.D. Hyde, Fungal Diversity 96: 159 (2019) Figure 2 and Figure 3
MycoBank: MB 555407
Saprobic on dead branches of bamboo in terrestrial habitat. Sexual morph: Undetermined. Asexual morph: hyphomycetous (Figure 2 and Figure 3). Colonies sporodochial, scattered, punctiform, pulvinate, granular, black, glistening. Mycelium immersed, consisting of branched, septate, thin-walled, smooth, pale to brown hyphae. Conidiophores up to 60 μm long, micronematous, mononematous, vesiculate, consisted of one to five subglobose to cylindrical, hyaline cells, smooth, unbranched, septate, constricted at the septa. Conidiogenous cells 8.5–12.5 × 7–10 µm ( = 9.8 × 8.8 µm, n = 10), holoblastic, monoblastic, integrated, terminal, determinate, subglobose, ellipsoidal, sometimes cuneiform, hyaline, smooth, thin-walled. Conidia 25–32 × 17–23 µm ( = 29 × 20 µm, n = 50), solitary, acrogenous, ellipsoidal to obovoid, muriform, smooth, brown, comprising of one straight column of vertical septa and three to four rows of transverse septa, slightly constricted at the septa, darkened and thickly banded at the septa, canals in the septa obscured by dark pigmentation; basal cell single, cuneiform, 4.5–6.5 µm wide, sometimes swollen, hyaline to pale brown.
Culture characteristics: Colonies on PDA reaching 20–30 mm after 5 months at 25 °C, circular, raised to umbonate, rough surface, dense, entire at the edge, brown, dry, reverse dark brown to black. Mycelium subhyaline to pale brown, 1.5–2.5 µm wide in culture. Conidiophores subhyaline. Conidiogenous cells integrated, subhyaline. Conidia pale brown to brown, septate, subglobose to obovoid, muriform, smooth, constricted at the septa, 20–25 µm ( = 22.5 µm, n = 30) long, 15–17 µm ( = 16.5 µm, n = 30) wide (Figure 3).
Material examined: CHINA, Sichuan Province, Chengdu City, Qionglai County, Chuanxi Bamboo Sea Area, 30°20′32″ N, 103°18′26″ E, 540 m elevation, on dead branches of bamboo in terrestrial habitat, 12 October 2021, X.D. Yu, A5 (HUEST 22.0057); living culture UESTCC 22.0056.
Notes: Canalisporium dehongense was introduced by Hyde et al. [46] from a submerged wood in Yunnan Province, China and has been considered as a later synonym of C. thailandense [47]. However, Goh and Kuo [48] treated Canalisporium dehongense and C. thailandense as distinct species, and this is followed in this study. The new collection clustered with Canalisporium dehongense in the single- and multi-gene phylogeny and share the similar conidiogenous cells and conidial morphology. Therefore, we identify our collection as C. dehongense, and an additional bamboo host record is provided herein.
Canalisporium sichuanense X.D. Yu, S.N. Zhang, and Jian K. Liu, sp. nov., Figure 4 and Figure 5
MycoBank: MB 847552
Etymology: The epithet refers to Sichuan Province where the fungus was collected.
Holotype: HKAS 124625
Saprobic on dead branches of bamboo in terrestrial habitat. Sexual morph: Undetermined. Asexual morph: hyphomycetous (Figure 4 and Figure 5). Colonies sporodochial, scattered, punctiform, pulvinate, granular, black, and shiny. Mycelium immersed, consisting of branched, septate, thin-walled, smooth, hyaline to pale brown hyphae. Conidiophores up to 60 µm long, micronematous, mononematous, vesiculate, consisted of one to six subglobose to cylindrical, hyaline cells, smooth, unbranched, septate, constricted at the septa. Conidiogenous cells 11–16 × 8–10 µm ( = 13.5 × 9 µm, n = 10), holoblastic, monoblastic, integrated, determinate, terminal, cylindrical, sometimes swelling to subglobose, hyaline, smooth, thin-walled. Conidia 27–37 × 17–21 µm ( = 31 × 20 µm, n = 50), solitary, acrogenous, cylindrical to obovoid, muriform, smooth, brown, comprising of a single, straight column of vertical septa and two to four rows of transverse septa, slightly constricted at the septa, darkened and thickly banded at the septa, canals in the septa obscured by dark pigmentation; basal cell cuneiform, 5.0–7.0 µm wide, sometimes swollen, hyaline to pale brown.
Culture characteristics: Colonies on PDA reaching 5–10 mm after 3 months at 25 °C, irregular, raised to umbonate, surface rough, dense, greyish-white, dry, reverse dark brown. Mycelium subhyaline to pale brown, 1.5–2.5 µm wide in culture. Conidiophores (Figure 5) subhyaline, 10–35 × 3.5–10.5 µm ( = 20.0 × 6.5 µm, n = 10). Conidiogenous cells (Figure 5) integrated, subhyaline, 4.5–10.5 × 5.5–10.5 µm ( = 8 × 7.5 µm, n = 10). Conidia (Figure 5) pale brown to brown, septate, cylindrical to obovoid, muriform, smooth, constricted at the septa, and the septa becoming progressively darker with conidial maturity, 15–24 µm ( = 20.5 µm, n = 30) long × 9–15 µm ( = 12.0 µm, n = 30) wide.
Material examined: CHINA, Sichuan Province, Chengdu City, Qionglai County, Lugou Bamboo Sea Area, 30°22′37″ N, 103°16′45″ E, 730 m elevation, on dead branches of bamboo in a terrestrial habitat, 12 October 2021, X.D. Yu, A44 (HKAS 124625, holotype); ex-type living culture CGMCC 3.23926; Dujiangyan County, Qingcheng Mountain, 30°54′29″ N, 103°32′36″ E, 960 m elevation, on dead branches of bamboo in a terrestrial habitat, 02 December 2021, Y. Yang, Q10-4 (HUEST 22.0061, paratype); ex-paratype living culture UESTCC 22.0060.
Notes: Morphologically, Canalisporium sichuanense resembles C. dehongense and C. thailandense in having hyaline, septate conidiophores, holoblastic, monoblastic conidiogenous cells, and muriform conidia [46,49]. However, they can be distinguished by the size of the basal cell (ca. 4 μm long in C. sichuanense, ca. 5 μm long in C. dehongense, ca. 2 μm long in C. thailandense) and conidial size (27–37 × 17–21 μm in C. sichuanense, 20–30 × 12–19 μm in C. dehongense, 22.5–31 × 17–22 μm in C. thailandense) [46,49]. Phylogenetically, they are distinct from each other (Figure 1), of which C. sichuanense is closer and sister to C. dehongense with high statistical support (100% ML/1.00 BYPP). The comparison of nucleotide differences between C. sichuanense and C. dehongense (MFLUCC 18-1396) showed that there are 0.10% (1/970) differences in SSU, 6.69% (44/658, including six gaps) in ITS, and 1.45% (11/761) in LSU gene regions, which also supports the introduction of C. sichuanense as a new species.
Dematiosporium aquaticum Z.L. Luo, K.D. Hyde, and H.Y. Su, Fungal Diversity 99: 573 (2019) Figure 6
MycoBank: MB 555673
Saprobic on dead bamboo in freshwater habitat. Sexual morph: Undetermined. Asexual morph: hyphomycetous. Colonies on natural substratum, effuse, scattered to gregarious, dark brown to black, glistening, superficial. Mycelium immersed in natural substrate, unbranched, septate, hyaline to subhyaline hyphae. Conidiophores reduced to conidiogenous cells, or rarely 20–30 × 3.5–4.5 µm, micronematous, mononematous, cylindrical, unbranched. Conidiogenous cells not observed. Conidia 21–28 µm diam ( = 25 µm, n = 50), solitary, acrogenous, globose to subglobose, brown to dark brown, dictyospores, slightly constricted at the septa, with a pore in each cell.
Culture characteristics: Colonies on PDA reaching 10–15 mm after 7 months at 25 °C, circular, with dense mycelium on the surface, dark grayish of the inner ring, and brown.
Material examined: CHINA, Sichuan Province, Chengdu City, Qionglai County, Lugou Bamboo Sea Area, 30°22′37″ N, 103°16′45″ E, 730 m elevation, on dead branches of bamboo in a freshwater habitat, 12 October 2021, X.D. Yu, A1 (HUEST 22.0056); living culture UESTCC 22.0055.
Notes: Luo et al. [26] introduced a monotypic genus Dematiosporium, which was collected from decaying submerged wood in Erhai lake, Dali City, Yunnan Province, China. Subsequently, Réblová et al. [17] recollected and described it in France, where it occurs on decaying submerged wood of Alnus glutinosa and other unidentified substrates. Species of Dematiosporium are often found on decaying wood in aquatic environments and it is characterized by cylindrical, unbranched, aseptate conidiophores and globose to subglobose, dictyospores conidia with a pore in each cell [17,26]. Our new collection was found from decaying bamboo in freshwater environments. We identify it as D. aquaticum based on the morphological characters and phylogenetic analyses. The SSU, ITS, rpb2, and tef1α regions were attempted, and we were able to obtain the LSU sequences. This is the first report of D. aquaticum from bamboo in a freshwater habitat. We describe D. aquaticum in detail and supplement the description of the conidiophore that was missing from the previous description.
Dematiosporium bambusicola X.D. Yu, S.N. Zhang, and Jian K. Liu, sp. nov., Figure 7.
MycoBank: MB 847553
Etymology: Refers to the bamboo host from which the fungi was found.
Holotype: HKAS 124626
Saprobic on dead bamboo in freshwater habitat. Sexual morph: Undetermined. Asexual morph: hyphomycetous. Colonies on natural substratum, effuse, scattered to gregarious, dark brown to black, glistening, superficial. Mycelium immersed in natural substrate, composed of hyaline, septate, branched, smooth hyphae. Conidiophores 6.5–11.5 × 2–4.5 µm ( = 9 × 3 µm, n = 10), micronematous, mononematous, cylindrical, straight or slightly flexuous, unbranched, aseptate. Conidiogenous cells holoblastic, monoblastic, cuneiform, integrated, terminal, determinate, hyaline. Conidia 35–60 × 27–41 µm ( = 46 × 34 µm, n = 50), solitary, acrogenous, ellipsoidal to subglobose, dark brown to black, smooth-walled, dictyospores, with a pore in each cell (Figure 7j), broadly rounded at apex, subtruncate at the base.
Culture characteristics: Colonies on PDA reaching 30–40 mm after 4 months at 25℃, circular, with sparse mycelium on the surface, slightly raised, umbonate, greyish-green, and reverse dark brown to black.
Material examined: CHINA, Sichuan Province, Chengdu City, Qionglai County, Lugou Bamboo Sea Area, 30°22′37″ N, 103°16′45″ E, 730m elevation, on dead branches of bamboo in freshwater habitat, 12 October 2021, X.D. Yu, A22 (HKAS 124626, holotype); ex-type living culture CGMCC 3.23774, living culture UESTCC 22.0058, UESTCC 22.0059.
Notes: The phylogenetic analyses showed that three isolates of Dematiosporium bambusicola formed a monophyletic clade in Savoryellaceae and are sister to D. aquaticum with absolute statistical support (100% ML/1.00 BYPP). Dematiosporium Bambusicola resembles D. aquaticum in forming dematiaceous, dictyospores conidia with a pore [26]. However, D. bambusicola has larger conidia than that of D. aquaticus (35–60 × 27–41 µm vs. 21–28 µm diam) [26]. The conidia of D. bambusicola are ellipsoidal to subglobose and dark brown to nearly black, while D. aquaticus has globose to subglobose conidia and brown to dark brown [26]. In addition, D. bambusicola differs from the latter in having smaller conidiophores (6.5–11.5 × 2–4.5 µm vs. 20–30 × 3.5–4.5 µm) [26]. We hereby introduce the new species based on the distinctiveness of morphology and multi-gene phylogeny.
Savoryella bambusicola X.D. Yu, S.N. Zhang, and Jian K. Liu, sp. nov., Figure 8.
MycoBank: MB 847554
Etymology: Refers to the bamboo host from which the fungi was found.
Holotype: HKAS 124627
Saprobic on dead bamboo in freshwater habitat. Sexual morph: Ascomata 270–350 μm high, 180–210 μm diam., scattered or solitary, superficial, black, ellipsoidal, uniloculate, thin-walled, laterally ostiolate, lying horizontal to the host surface with a short, brown neck. Peridium comprising several layers of brown, thick-walled cells of textura epidermoidea. Paraphyses 4.5–6.5 µm wide, numerous, cylindrical, and somehow swollen, branched, hyaline, septate, constricted at the septa. Asci 90–130 × 19–23 µm ( = 119 × 21 µm, n = 30), 8-spored, unitunicate, cylindric-clavate, straight or slightly curved, short pedicellate, rounded at the apex, with an apical truncate non-amyloid apical thickening containing a pore. Ascospores 24.5–36.5 × 9–12 µm ( = 30.5 × 10.5 µm, n = 50), uni- or biseriate, straight or slightly curved, fusiform, three-septate, constricted and thickened at the septa, central cells larger and brown, apical cells smaller and hyaline, thin-walled, without sheaths or appendages. Asexual morph: Undetermined.
Culture characteristics: Colonies on PDA reaching 10–15 mm after 2 months at 25 °C, circular, with dense mycelium on the surface, light gray of the inner ring, and light yellow of the outer ring; in reverse black.
Material examined: CHINA, Sichuan Province, Chengdu City, Qionglai County, Lugou Bamboo Sea Area, 30°22′37″ N, 103°16′45″ E, 730m elevation, on dead branches of bamboo in freshwater habitat, 12 October 2021, X.D. Yu, A23 (HKAS 124627, holotype); ex-type living culture CGMCC 3.23775, ibid., A20 (HUEST 22.0058, isotype); ex-isotype living culture UESTCC 22.0057.
Notes: The phylogenetic result based on SSU, ITS, LSU, rpb2, and tef1α sequence data showed that the new collections Savoryella bambusicola nested in Savoryella and formed a distinct lineage (Figure 1). Morphologically, S. bambusicola resembles S. curvispora and S. fusiformis in having eight-spored asci, fusiform, three-septate ascospores [29]. However, they can be recognized as different species; Savoryella bambusicola differs from S. curvispora and S. fusiformis in having relatively broader asci (90–130 × 19–23 vs. 90–115 × 15–17 vs. 80–120 × 9–14) and ascospores (24.5–36.5 × 9–12 vs. 25–28 × 7–10 vs. 25–35 × 6–9.6) [29]. The establishment of the new species S. bambusicola is justified by morphological and phylogenetic evidence.
4. Discussion
Tibpromma et al. [20] introduced Canalisporium krabiense and C. thailandense from Thailand. These two species have different conidiogenous cells, but were found to have almost identical ITS and LSU sequences and were phylogenetically clustered together (Figure 1). Koukol and Delgado [47] speculated that DNA cross-contamination happened between C. krabiense and C. thailandense. Furthermore, they provided synonymy of another species C. dehongense under C. thailandense. In this study, we deem it as a speculative inference and do not follow this treatment with the following concerns: (1) in Koukol and Delgado [47], the globose to oval conidiogenous cells connected in a chain of C. dehongense and C. thailandense was also observed in other incorrectly identified C. caribense; and inferring from this, they speculated that C. thailandense is worldwide and C. dehongense could be a further record; (2) the synonymy of C. dehongense under C. thailandense is only based on morphology; since C. dehongense and C. thailandense are represented by a single specimen at that time, there was no further evidence to refute the inference [20,46,47]; (3) additional collection of C. dehongense is provided in this study (HUEST 22.0057; UESTCC 22.0056), which supported and validated the initial identification of C. dehongense in Hyde et al. [46]; (4) Goh and Kuo [48] also pointed out that C. dehongense and C. thailandense (the basal cell ca. 5µm long vs. 2µm long) are distinct species due to morpho-phylogenetical distinction.
Species of Savoryellaceae have been found on various hosts in aquatic and terrestrial habitats [16], i.e., Ascotaiwania mauritiana on Pandanus palustris (Pandanaceae) [50], Ascotaiwania palmicola on Iriartea sp. (Arecaceae) [51], Savoryella aquatica on Machilus sp. (Lauraceae) [21], Savoryella lignicola on Bambusa sp. (Poaceae) [21], Savoryella nypae on Nypa fruticans (Arecaceae) [19], Savoryella paucispora on Pinus sp. (Pinaceae) [22]. Freshwater species are accommodated in all the genera in Savoryellaceae: Ascotaiwania (6 species) [50,52,53,54], Bactrodesmium (6 species) [17,55], Canalisporium (17 species) [27,28,46,48,56,57,58,59,60], Dematiosporium (1 species) [26], Neoascotaiwania (4 species) [23,52,61,62], and Savoryella (9 species) [16,19,21,29,63]. It seems the members of this family are more likely to be found from monocotyledons and favorable to hard tissue substrates in freshwater habitats.
Asexual morphs have been found in all six genera in Savoryellaceae, of which Bactrodesmium and Dematiosporium are represented only by asexual morphs; members of Canalisporium mostly are asexual morphs with only C. grenadoideum having a holomorph; while Savoryella is commonly known as a sexual morph with only S. nypae and S. sarushimana represented by a trichocladium-like asexual morph [19]; Ascotaiwania and Neoascotaiwania both have holomorphs, but different in asexual morphs (monodictys-like, monotosporella-like, and trichocladium-like vs. bactrodesmium-like) [53,62,64,65,66]. In this study, one sexual morph of Savoryella and four asexual morphs of Canalisporium and Dematiosporium are isolated and identified, which contributed to the taxonomy of Savoryellaceae and the diversity of bambusicolous fungi.
Conceptualization, X.-D.Y., S.-N.Z. and J.-K.L.; methodology, X.-D.Y. and J.-K.L.; formal analysis, X.-D.Y. and S.-N.Z.; resources, X.-D.Y. and J.-K.L.; data curation, X.-D.Y. and S.-N.Z.; writing—original draft preparation, X.-D.Y.; writing—review and editing, X.-D.Y., S.-N.Z. and J.-K.L.; supervision, J.-K.L.; project administration, J.-K.L.; funding acquisition, J.-K.L. All authors have read and agreed to the published version of the manuscript.
Not applicable.
Not applicable.
The sequences and alignments data were submitted to GenBank and TreeBASE, respectively.
Xiang Ma, Yi Yang and Jing-Yi Song are thanked for their help with sample collection.
The authors declare no conflict of interest.
Footnotes
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Figure 1. RAxML tree generated from combined SSU, ITS, LSU, rpb2, and tef1α sequence data of Savoryellaceae. Bootstrap values for ML equal to or greater than 75% are placed above the branches. Branches with Bayesian posterior probabilities (BYPP) from MCMC analysis equal to or greater than 0.95 were in bold. The ex-type strains were indicated in bold, and newly generated sequences were indicated in red. “T” represents the type species of each genus.
Figure 2. Canalisporium dehongense (HUEST 22.0057) (a–c) colonies on bamboo substrate. (d–g) Conidiophores and conidia. (h–l) Conidia with conidiogenous cells. (m,n) Colonies on PDA, above (m) and below (n). Scale bars: (d–l) = 10 μm.
Figure 3. Asexual reproduction of Canalisporium dehongense (UESTCC 22.0056) on PDA medium about three months. (a) Hyphae and conidiophores with conidia. (b–h) Conidiogenous cells and conidia. (i–n) Conidia. Scale bars: (a–f) = 20 μm, (g–n) = 10 μm.
Figure 4. Canalisporium sichuanense (HKAS 124625, holotype) (a–h) colonies on natural substrate. (a,b) Sporodochia on a bamboo substrate. (c) Squash mount of sporodochium showing conidiophores and conidia. (d) Conidiophores comprising of vesiculate cells. (e–h) Conidia with conidiogenous cells. (i,j) Colonies on PDA, above (i) and below (j). Scale bars: (c) = 50 μm, (d) = 20 μm, (e–h) = 10 μm.
Figure 5. Asexual reproduction of Canalisporium sichuanense (CGMCC 3.23926, ex-type) on PDA medium about three months. (a,b) Hyphae and conidiophores with conidia. (c–i) Conidiogenous cells and conidia. Scale bars: (a,b) = 50 μm, (c–i) = 10 μm.
Figure 6. Dematiosporium aquaticum (HUEST 22.0056) (a,b) colonies on bamboo substrate. (c) Conidiophores and conidia. (d–f) Conidia. (g) Fragile conidium. (h) Germinating conidium. (i,j) Colonies on PDA, above (i) and below (j). Scale bars: (c–h) = 10 μm.
Figure 7. Dematiosporium bambusicola (HKAS 124626, holotype) (a,b) colonies on a bamboo substrate. (c–e) Conidiophores and conidia. (f–j) Conidia. (j) The arrow indicated pore. (k) Germinating conidium. (l,m) Colonies on PDA, above (l) and below (m). Scale bars: (c–k) = 20 μm.
Figure 8. Savoryella bambusicola (HKAS 124627, holotype) (a,b) ascomata on host substrate. (c) Neck. (d) Squash mounts of ascomata. (e,f) Peridium. (g) Paraphyses. (h) Apical ring. (i–l) Asci. (m–p) Ascospores. (q,r) Colonies on PDA, above (q) and below (r). Scale bars: (c) = 50 μm, (d) = 100 μm, (e–g,i–l) = 20 μm, (m–p) = 10 μm, (h) = 5 μm.
Taxa used in the phylogenetic analyses and their GenBank accession numbers. Newly generated sequences are indicated with * and the ex-type strains are in bold. “N/A” sequence is unavailable.
Taxa | Vouchers/Strains/Isolates | GenBank Accession Numbers | ||||
---|---|---|---|---|---|---|
SSU | ITS | LSU | rpb2 | tef1α | ||
Ascotaiwania latericolla | ICMP 22739 | N/A | MN699390 | MN699407 | MN704312 | N/A |
Ascotaiwania lignicola | NIL 00005 | HQ446284 | HQ446341 | HQ446364 | HQ446419 | HQ446307 |
Ascotaiwania lignicola | NIL 00006 | HQ446285 | HQ446342 | HQ446365 | N/A | HQ446308 |
Ascotaiwania mitriformis | HKUCC 3706 | N/A | N/A | AF132324 | N/A | N/A |
Ascotaiwania sawadae | SS 00051 | HQ446283 | HQ446340 | HQ446363 | HQ446418 | HQ446306 |
Ascotaiwania uniseptata | Sloan 5406 | N/A | N/A | KT278718 | N/A | N/A |
Bactrodesmium abruptum | CBS 144404 | MN699365 | MN699391 | MN699408 | MN704288 | MN704313 |
Bactrodesmium diversum | CBS 142448 | MN699369 | MN699352 | MN699412 | MN704292 | MN704317 |
Bactrodesmium leptopus | CBS 144542 | MN699374 | MN699388 | MN699423 | MN704297 | MN704321 |
Bactrodesmium obovatum | CBS 144077 | MN699375 | MN699395 | MN699424 | MN704298 | MN704322 |
Bactrodesmium pallidum | CBS 142449 | MN699379 | MN699363 | MN699428 | MN704301 | MN704326 |
Bactrodesmium spilomeum | CBS 146104 | MN699381 | N/A | N/A | MN704303 | MN704328 |
Canalisporium aquaticium | MFLUCC 16-0862 | MN061353 | MN061351 | MN061365 | N/A | N/A |
Canalisporium caribense | SS 03839 | GQ390253 | GQ390283 | GQ390268 | HQ446421 | N/A |
Canalisporium dehongense * | UESTCC 22.0056 | OQ428250 | OQ428266 | OQ428258 | OQ437183 | OQ437176 |
Canalisporium dehongense | MFLUCC 18-1396 | MK051035 | MK051033 | MK051034 | N/A | N/A |
Canalisporium elegans | SS 00523 | GQ390255 | GQ390285 | GQ390270 | HQ446423 | HQ446310 |
Canalisporium exiguum | SS 00809 | GQ390266 | GQ390296 | GQ390281 | HQ446436 | N/A |
Canalisporium grenadoideum | SS 03615 | GQ390252 | GQ390282 | GQ390267 | HQ446420 | HQ446309 |
Canalisporium jinghongense | SS 03491 | GQ390257 | GQ390287 | GQ390272 | HQ446426 | HQ446313 |
Canalisporium kenyense | MFLU17-1086 | N/A | MH701998 | MH701999 | N/A | MH708885 |
Canalisporium krabiense | MFLU 16-1888 | N/A | MH275051 | MH260283 | N/A | N/A |
Canalisporium pallidum | SS 00498 | GQ390265 | GQ390295 | GQ390280 | HQ446435 | HQ446322 |
Canalisporium paulopallidum | NCYU-106A2-3-1 | N/A | MT946658 | N/A | N/A | N/A |
Canalisporium paulopallidum | NCYU-106A2-3-2 | N/A | MT946659 | N/A | N/A | N/A |
Canalisporium pulchrum | SS 03773 | GQ390263 | GQ390293 | GQ390278 | HQ446432 | HQ446319 |
Canalisporium sichuanense * | CGMCC 3.23926 | OQ428254 | OQ428270 | OQ428262 | OQ437186 | OQ437180 |
Canalisporium sichuanense * | UESTCC 22.0060 | OQ428255 | OQ428271 | OQ428263 | N/A | N/A |
Canalisporium taiwanense | NCYU-108ZQ-D1-1-1 | N/A | MT946663 | N/A | N/A | N/A |
Canalisporium taiwanense | NCYU-108ZQ-D1-1-2 | N/A | MT946664 | N/A | N/A | N/A |
‘Canalisporium thailandense’ | MFLU 16-1900 | N/A | MH275052 | MH260284 | N/A | N/A |
Dematiosporium aquaticum | CBS 144793 | MN699385 | MN699402 | MN699433 | MN704307 | MN704330 |
Dematiosporium aquaticum | MFLU 18-1641 | N/A | N/A | MK835855 | MN194029 | MN200286 |
Dematiosporium aquaticum * | UESTCC 22.0055 | N/A | N/A | OQ428257 | N/A | N/A |
Dematiosporium bambusicola * | CGMCC 3.23774 | OQ428252 | OQ428268 | OQ428260 | N/A | OQ437178 |
Dematiosporium bambusicola * | UESTCC 22.0058 | N/A | OQ428272 | OQ428264 | N/A | OQ437181 |
Dematiosporium bambusicola * | UESTCC 22.0059 | OQ428256 | OQ428273 | OQ428265 | N/A | OQ437182 |
Neoascotaiwania fusiformis | MFLUCC 15-0621 | N/A | MG388215 | KX550893 | KX576871 | N/A |
Neoascotaiwania limnetica | CBS 126576 | KT278689 | KY853452 | KY853513 | MN704308 | MN704331 |
Neoascotaiwania terrestris | CBS 142291 | KY853547 | KY853454 | KY853515 | N/A | N/A |
Pleurotheciella aquatica | MFLUCC 17-0464 | MF399220 | MF399236 | MF399253 | MF401405 | N/A |
Pleurotheciella erumpens | CBS 142447 | MN699387 | MN699406 | MN699435 | MN704311 | MN704334 |
Savoryella appendiculata | NF 00206 | HQ446293 | HQ446350 | N/A | HQ446442 | HQ446327 |
Savoryella aquatica | SS 03801 | HQ446292 | HQ446349 | HQ446372 | HQ446441 | HQ446326 |
Savoryella bambusicola * | CGMCC 3.23775 | OQ428253 | OQ428269 | OQ428261 | OQ437185 | OQ437179 |
Savoryella bambusicola * | UESTCC 22.0057 | OQ428251 | OQ428267 | OQ428259 | OQ437184 | OQ437177 |
Savoryella fusiformis | SS 00783 | HQ446294 | HQ446351 | N/A | HQ446443 | HQ446328 |
Savoryella lignicola | NF 00204 | HQ446300 | HQ446357 | HQ446378 | N/A | HQ446334 |
Savoryella longispora | SAT 00320 | HQ446301 | HQ446358 | HQ446379 | HQ446449 | HQ446335 |
Savoryella nypae | MFLUCC 18-1570 | MK543237 | MK543219 | MK543210 | N/A | MK542516 |
Savoryella paucispora | SAT 00867 | HQ446304 | HQ446361 | HQ446382 | HQ446452 | HQ446338 |
Savoryella sarushimana | NBRC 105262 | MK411005 | N/A | MK411004 | N/A | N/A |
Savoryella sp. | NF 00205 | HQ446305 | HQ446362 | N/A | N/A | HQ446339 |
Savoryella verrucosa | SS 03331 | HQ446298 | HQ446355 | HQ446376 | HQ446447 | HQ446332 |
Savoryella yunnanensis | MFLUCC 18-1395 | MK411423 | N/A | MK411422 | N/A | MK411424 |
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Abstract
Asexual and sexual morphs of saprobic bambusicolous fungi were collected from freshwater and terrestrial habitats in Sichuan Province, China. Taxonomic identification of these fungi was carried out on the basis of morphological comparison, culture characteristics, and molecular phylogeny. Multi-gene phylogeny based on combined SSU, ITS, LSU, rpb2, and tef1α sequence data was performed to determine their phylogenetic placement, and the result showed that these fungi belong to Savoryellaceae. Morphologically, four asexual morphs are similar to Canalisporium and Dematiosporium, while a sexual morph well-fits to Savoryella. Three new species, Canalisporium sichuanense, Dematiosporium bambusicola, and Savoryella bambusicola are identified and described. Two new records, C. dehongense and D. aquaticum, were recovered from the bamboo hosts in terrestrial and freshwater habitats, respectively. In addition, the nomenclatural confusion of C. dehongense and C. thailandense is discussed.
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