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Research Article
Two new species and one new combination of Ophiocordyceps (Hypocreales, Ophiocordycipitaceae) in Guizhou
expand article infoXing-Can Peng‡§|, Ting-Chi Wen§, De-Ping Wei§, Yu-Hong Liao#¤, Yi Wang§, Xian Zhang§|, Gui-Ying Wang§, Yun Zhou§, Khanobporn Tangtrakulwanich|, Jian-Dong Liang‡
‡ Guizhou University of Traditional Chinese Medicine, Guiyang, China
§ Guizhou University, Guizhou, China
| Mae Fah Luang University, Chiang Rai, Thailand
¶ Guizhou Key Laboratory of Edible Fungi Breeding, Guiyang, China
# Shenzhen Ainiang Biotechnology Co., Ltd., Shenzhen, China
¤ Shenzhen Longgang Buji Middle School, Shenzhen, China

Corresponding author: Jian-Dong Liang ( cordyceps2005@qq.com )

Academic editor: Marc Stadler
© 2024 Xing-Can Peng, Ting-Chi Wen, De-Ping Wei, Yu-Hong Liao, Yi Wang, Xian Zhang, Gui-Ying Wang, Yun Zhou, Khanobporn Tangtrakulwanich, Jian-Dong Liang.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Peng X-C, Wen T-C, Wei D-P, Liao Y-H, Wang Y, Zhang X, Wang G-Y, Zhou Y, Tangtrakulwanich K, Liang J-D (2024) Two new species and one new combination of Ophiocordyceps (Hypocreales, Ophiocordycipitaceae) in Guizhou. MycoKeys 102: 245-266. https://doi.org/10.3897/mycokeys.102.113351
Open Access

Abstract

Ophiocordyceps is the largest genus in Ophiocordycipitaceae and has a broad distribution with high diversity in subtropical and tropical regions. In this study, two new species, pathogenic on lepidopteran larvae are introduced, based on morphological observation and molecular phylogeny. Ophiocordyceps fenggangensis sp. nov. is characterised by having fibrous, stalked stroma with a sterile tip, immersed perithecia, cylindrical asci and filiform ascospores disarticulating into secondary spores. Ophiocordyceps liangii sp. nov. has the characteristics of fibrous, brown, stipitate, filiform stroma, superficial perithecia, cylindrical asci and cylindrical-filiform, non-disarticulating ascospores. A new combination Ophiocordyceps musicaudata (syn. Cordyceps musicaudata) is established employing molecular analysis and morphological characteristics. Ophiocordyceps musicaudata is characterised by wiry, stipitate, solitary, paired to multiple stromata, yellowish, branched fertile part, brown stipe, immersed perithecia, cylindrical asci and cylindrical-filiform, non-disarticulating ascospores.

Key words

Entomopathogenic fungi>, morphology, phylogenetic, two new taxa

Introduction

Hypocreales is a fungal order enriched in arthropod-pathogens, which are taxonomically placed in Clavicipitaceae, Cordycipitaceae, Ophiocordycipitaceae and Polycephalomycetaceae (Luangsa-Ard et al. 2018; Wei et al. 2021a; Xiao et al. 2023). Entomopathogens in these four families can infect many orders of insects and arachnids (Luangsa-Ard et al. 2018; Wei et al. 2022). Hypocrealean entomopathogens can infect various developmental stages of the insect, from larva, pupa to nymph and adults (Luangsa-Ard et al. 2018). For example, Ophiocordyceps acicularis is a parasite on larvae of Coleoptera (Sung et al. 2007), Cordyceps morakotii on pupa of Hymenoptera (Tasanathai et al. 2016), Cordyceps cocoonihabita on cocoons of Lepidoptera (Wang et al. 2020), Ophiocordyceps asiana on adults of Hemiptera (Khao-ngam et al. 2021), Ophiocordyceps dipterigena on adults of Diptera (Quandt et al. 2014) and Simplicillium yunnanense on the Araneae (Wang et al. 2020).

Ophiocordycipitaceae contains more than 500 species and about three out of five species are distributed in its type genus Ophiocordyceps. Ophiocordyceps was established by Petch (1931) to accommodate four species with non-disarticulating ascospores, as well as clavate asci with thickened apices: Ophiocordyceps blattae, O. unilateralis, O. rhizoidea and O. peltata. Subsequently, an increasing number of species were transferred from Cordyceps into Ophiocordyceps (Sung et al. 2007; Quandt et al. 2014). Ophiocordyceps are characterised by dark, fibrous, wiry, pliant stromata, superficial to completely immersed perithecia, cylindrical asci with thickened cap, fusiform to filiform ascospores disarticulating or non-disarticulating (Sung et al. 2007; Xiao et al. 2019). The asexual genera associated with Ophiocordyceps are Hirsutella, Hymenostilbe, Paraisaria, Stilbella and Syngliocladium (Sung et al. 2007; Quandt et al. 2014; Yang et al. 2021). By employing multigene phylogeny, Quandt et al. (2014) updated the generic composition of Ophiocordycipitaceae and accepted Drechmeria, Harposporium, Ophiocordyceps, Polycephalomyces, Purpureocillium and Tolypocladium in this family; meanwhile, twelve genera including Cordycepioideus, Didymobotryopsis, Didymobotrys, Hirsutella, Hymenostilbe, Mahevia, Paraisaria, Sorosporella, Syngliocladium, Synnematium, Trichosterigma and Troglobiomyces were rejected in favour of Ophiocordyceps, following the principle of “one fungus one name”. Mongkolsamrit et al. (2019) resurrected the genus Paraisaria in Ophiocordycipitaceae. Crous et al. (2020) and Araújo et al. (2022) established Hantamomyces and Torrubiellomyces, respectively. Xiao et al. (2023) transferred Polycephalomyces, Perennicordyceps and Pleurocordyceps from Ophiocordycipitaceae to a new family, Polycephalomycetaceae, based on biphasic analyses. Therefore, Ophiocordycipitaceae currently contains eight genera, namely Drechmeria, Hantamomyces, Harposporium, Ophiocordyceps, Paraisaria, Purpureocillium, Tolypocladium and Torrubiellomyces.

In this study, we collected three entomoapthogenic fungi> from lepidoptera larvae found in disturbed forests in Guizhou Province, China. These specimens have typical characters of Ophiocordyceps in terms of the macro- and micro-morphologies. This study attempts to reveal their taxonomic placements, based on morphological characteristics and molecular analysis of the combined LSU, ITS, SSU, tef1-α, rpb1 and rpb2 dataset.

Materials and methods

Collection, isolation and morphological study

Specimens were scanned from the ground of disturbed forests in Guizhou Province, China. Three species were found to infect lepidopteran larvae and their stromata protruded from the ground. Amongst them, the hosts of specimen HKAS 125848 were found completely immersed into soil. The host of specimen GACP SY22072880 was found semi-immersed into soil. The specimen HKAS 125845 was found on leaf litter. Macro-morphological characteristics of fresh collections were documented with a camera (Canon 6D) and locations were recorded with Biotracks in the field. The specimens were collected into a plastic box and transported to the laboratory for subsequent studies. The culture of the specimens was obtained by transferring a small mass of mycelium inside the body of the host into potato dextrose agar (PDA) using a sterile inoculation needle and incubated at 25 °C (Wei et al. 2021b). A Leica stereomicroscope (Leica S9E) was used to examine and section the fruiting bodies. Sections of fertile head were mounted on glass slides with a drop of ultrapure water and covered with a cover slip. A Leica compound microscope (Leica DM2500) was used to photograph and measure perithecia, asci, peridium, apical cap, ascospores and secondary ascospores. The fruiting bodies were dried with allochroic silica gel and deposited in the Herbarium of Cryptogams, Kunming Institute of Botany of the Chinese Academy of Sciences (KUN-HKAS), the cultures being deposited in the Herbarium of Guizhou University (GACP).

DNA extraction, PCR amplification and sequencing

DNA was extracted from mycelium inside the body of insect hosts and from fresh mycelium on PDA medium using DNA extraction kit (Fungal gDNA Isolation Kit, Biomiga, CA, USA), following the protocol of the manufacturer. The obtained total genomic DNA was stored at -20 °C. Six loci including the partial large subunit rRNA gene (LSU), internal transcribed spacer including the 5.8S rDNA gene (ITS), the partial small subunit rRNA gene (SSU), the translation elongation factor 1-alpha gene (tef1-α), the partial RNA polymerase II largest subunit (rpb1) and the partial RNA polymerase II second largest subunit (rpb2) were amplified and sequenced. The primers LROR/LR5 were used for LSU (Vilgalys and Hester 1990), ITS5/ITS4 for ITS (White et al. 1990), NS1/NS4 for SSU (White et al. 1990), EF1-983F/EF1-2218R for tef1-α (Rehner and Buckley 2005), CRPB1A/RPB1Cr for rpb1 (Castlebury et al. 2004) and fRPB2-5f/fRPB2-7cR for rpb2 (Castlebury et al. 2004). The Polymerase Chain Reaction (PCR) was performed in a 50 µl volumes consisting of 22 µl PCR mixture (2× Taq PCR StarMix with Loading Dye, GenStar) which contains Taq DNA polymerase, dNTPs, Mg2+, a reaction buffer and stabiliser, 20 µl of double distilled water, 2 µl of each primer and 4 µl of DNA template. Amplifications were carried out using a BioRAD T100 Thermal Cycler (Singapore) with the following conditions: (1) initialisation at 94 °C for 3 min, for ITS (2) 33 cycles of denaturation at 94 °C for 30 sec, annealing at 51 °C for 50 sec and extension at 72 °C for 45 sec; for SSU and LSU (2) 33 cycles of denaturation at 94 °C for 30 sec, annealing at 50 °C for 30 sec and extension at 72 °C for 2 min; for tef1-α (2) 33 cycles of denaturation at 94 °C for 30 sec, annealing at 58 °C for 50 sec and extension at 72 °C for 1 min; for rpb1 and rpb2 (2) 33 cycles of denaturation at 94 °C for 30 sec, annealing at 51 °C for 40 sec and extension at 72 °C for 1 min 20 sec and followed by (3) final extension at 72 °C for 10 min. The PCR products were sent to Tsingke Biological Technology in Chongqing, China, for sequencing using the above primers. The generated sequences were edited manually for excluding ambiguous region with BioEdit v.7.0.5.3 (Hall et al. 2011). The accession numbers and hosts are listed in Table 1.

Table 1.
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GenBank accession numbers of the taxa used in the phylogenetic analyses, the newly- generated sequences are in bold, T Represents type strain, type specimens or neotype.

Current name Voucher host LSU ITS SSU tef1-α rpb1 rpb2 References
Cordyceps militaris OSC 93623 Lepidoptera AY184966 JN049825 AY184977 DQ522332 DQ522377 AY545732 Kepler et al. 2012
YFCC 6587 MN576818 MN576762 MN576988 MN576878 MN576932 Wang et al. 2020
Drechmeria balanoides CBS 250.82T AF339539 AF339588 DQ522342 DQ522442 Sung et al. 2007
D. gunnii OSC 76404 Lepidoptera AF339522 JN049822 AF339572 AY489616 AY489650 DQ522426 Luangsa-Ard et al. 2018
D. panacis CBS 142798T Apiales MF588897 MF588878 MF588890 MF614144 Yeh et al. 2021
D. zeospora CBS 335.80T AF339540 MH861269 AF339589 EF469062 EF469091 EF469109 Vu et al. 2019
Harposporium anguillulae ARSEF 5593 AY636081 Chaverri et al. 2005
Har. cycloides ARSEF 5599 AY636083 Chaverri et al. 2005
Har. harposporiferum ARSEF 5472T NG_060621 AF339569 Sung et al. 2001
Har. helicoides ARSEF 5354 Nematode AF339527 AF339577 Sung et al. 2001
Hirsutella citriformis ARSEF1 035 Hemiptera KM652105 KM652153 KM652064 KM651989 KM652030 Simmons et al. 2015
ARSEF 1446 Hemiptera KM652106 KM652154 KM652065 KM651990 KM652031 Simmons et al. 2015
Hir. fusiformis ARSEF 5474 Coleoptera KM652110 KM652067 KM651993 KM652033 Simmons et al. 2015
Hir. gigantea ARSEF 30 Hymenoptera JX566977 JX566980 KM652034 Simmons et al. 2015
Hir. kuankuoshuiensis GZUIFR-2012KKS3-1 Lepidoptera KY415582 KY415575 KY415590 KY945360 Qu et al. 2021
Hir. radiata ARSEF 1369 Diptera KM652119 KM652076 KM652002 KM652042 Simmons et al. 2015
Hir. shennongjiaensis GZUIFR-Snj121022T Dermaptera KY945357 KT390721 KY945364 Zou et al. 2016
Ophiocordyceps acicularis OSC 110987 Coleoptera EF468805 EF468950 EF468744 EF468852 Sung et al. 2007
O. agriotidis ARSEF 5692 Coleoptera DQ518754 JN049819 DQ522540 DQ522322 DQ522368 DQ522418 Kepler et al. 2012
O. alboperitheciata YHH 16755T Lepidoptera MT222278 MT222279 MT222280 MT222281 Fan et al. 2021
O. appendiculata NBRC 106959 Coleoptera JN941412 JN943325 JN941729 AB968578 JN992463 AB968540 Ban et al. 2015
O. araracuarensis HUA 186135 Hemiptera KC610769 KP200891 KC610788 KC610738 KF658665 KC610716 Sanjuan et al. 2015
O. asiatica BCC 86435 Blattodea MH753676 MH754723 MK214106 MK214092 Tasanathai et al. 2019
O. bidoupensis YHH 20036T Coleoptera OK571396 OK556893 OK556897 OK556899 Zou et al. 2022
O. brunneiperitheciata TBRC 8100 Lepidoptera MF614658 MF614643 MF614685 Luangsa-Ard et al. 2018
BCC 49312 Lepidoptera MF614660 MF614642 MF614686 Luangsa-Ard et al. 2018
O. coccidiicola NBRC 100682 AB968419 AB968404 AB968391 AB968583 AB968545 Ban et al. 2015
O. communis BCC 1874 Blattodea MH753679 MH754725 MK284267 MK214109 MK214095 Tasanathai et al. 2019
O. crinalis GDGM 17327 Lepidoptera KF226254 KF226253 KF226256 KF226255 Wang et al. 2014
O. delicatula ARSEF 14442T Hemiptera MZ198251 MZ246828 MZ246829 Clifton et al. 2021
O. elongata OSC 110989 Lepidoptera EF468808 EF468748 EF468856 Sung et al. 2007
O. entomorrhiza KEW 53484 Lepidoptera EF468809 JN049850 EF468954 EF468749 EF468857 EF468911 Quandt et al. 2014
Ophiocordyceps fenggangensis HKAS 125848T Lepidoptera OR527542 OR527535 OR526346 OR526351 This study
GACP FG21042850 Lepidoptera OR527541 OR527534 OR527538 OR526345 OR526350 OR526353 This study
O. flabellata YFCC 8795T Hymenoptera OL310724 OL310721 OL322688 OL322687 OL322695 Tang et al. 2023b
O. formosana TNM F13893 Coleoptera KJ878908 KJ878956 KJ878988 KJ878943 Quandt et al. 2014
O. fusiformis BCC 93025T Blattodea MZ675422 MZ676743 MZ707849 MZ707855 MZ707805 Tasanathai et al. 2022
O. gracillima HUA 186132 Coleoptera KC610768 KF937353 KC610744 KF658666 Sanjuan et al. 2015
Ophiocordyceps liangii HKAS 125845T Lepidoptera OR527543 OR527536 OR527539 OR526347 This study
GACP LB22071253 Lepidoptera OR527544 OR527537 OR527540 OR526348 OR526354 This study
O. macroacicularis NBRC 105888 Lepidoptera AB968417 AB968401 AB968389 AB968575 AB968537 Ban et al. 2015
O. melolonthae OSC 110993 Coleoptera DQ518762 DQ522548 DQ522331 DQ522376 Spatafora et al. 2007
O. monacidis MF74 Hymenoptera KX713605 KX713647 KX713712 Araújo et al. 2018
O. mosingtoensis BCC 30904 Blattodea MH753686 MH754732 MK284273 MK214115 MK214100 Tasanathai et al. 2019
O. multiperitheciata BCC 22861 Lepidoptera MF614656 MF614640 MF614670 MF614683 Araújo et al. 2018
Ophiocordyceps musicaudata GACP SY22072879 Lepidoptera OR527545 OR526349 OR526352 This study
O. naomipierceae DAWKSANT Hymenoptera KX713589 KX713664 KX713701 Araújo et al. 2018
O. nigra TNS 16250 Coleoptera KJ878942 KJ878987 KJ879021 Quandt et al. 2014
O. nigrella EFCC 9247 Lepidoptera EF468818 JN049853 EF468963 EF468758 EF468866 EF468920 Sung et al. 2007
O. nooreniae BRIP 55363T Hymenoptera KX673810 KX673811 KX673812 KX673809 Crous et al. 2016
O. ovatospora YHH 2206001T Blattodea OP295113 OP295105 OP295110 OP313801 OP313803 OP313805 Tang et al. 2022
O. pseudocommunis BCC 16757 Blattodea MH753687 MH754733 MK284274 MK214117 MK214101 Tasanathai et al. 2019
O. pseudorhizoidea BCC 86431 Blattodea MH753674 MH754721 MK284262 MK751469 MK214090 Tasanathai et al. 2019
O. purpureostromata TNS F18430 Coleoptera KJ878897 KJ878931 KJ878977 KJ879011 Quandt et al. 2014
O. ravenelii OSC 110995 Coleoptera DQ518764 DQ522550 DQ522334 DQ522379 DQ522430 Spatafora et al. 2007
O. robertsii KEW 27083 Lepidoptera EF468826 EF468766 Sung et al. 2007
O. sinensis EFCC 7287 Lepidoptera EF468827 JN049854 EF468971 EF468767 EF468874 EF468924 Sung et al. 2007
O. spataforae OSC 128575 Hemiptera EF469079 JN049845 EF469126 EF469064 EF469093 EF469110 Sung et al. 2007
O. unilateralis OSC 128574 Hymenoptera DQ518768 DQ522554 DQ522339 DQ522385 DQ522436 Spatafora et al. 2007
Paraisaria amazonica HUA 186143 Orthoptera KJ917571 KJ917562 KM411989 KP212902 KM411982 Sanjuan et al. 2015
Par. blattarioides HUA 186093 Blattodea KJ917570 KJ917559 KM411992 KP212910 Sanjuan et al. 2015
HUA 186108 Blattodea KJ917569 KJ917558 KP212912 KM411984 Sanjuan et al. 2015
Par. coenomyiae NBRC 108993T Diptera AB968412 AB968396 AB968384 AB968570 AB968532 Ban et al. 2015
Par. gracilioides HUA 186092 Coleoptera KJ130992 KJ917555 KP212915 Araújo et al. 2018
Par. gracilis EFCC 3101 Lepidoptera EF468810 EF468955 EF468750 EF468858 EF468913 Araújo et al. 2018
Par. heteropoda EFCC 10125 Hemiptera EF468812 JN049852 EF468957 EF468752 EF468860 EF468914 Sung et al. 2007
Par. orthopterorum TBRC 9710 Orthoptera MK332582 MH754743 MK214081 MK214085 Mongkolsamrit et al. 2019
Par. phuwiangensis BBH 43491 Coleoptera MK192058 MH188542 MH211351 Mongkolsamrit et al. 2019
Par. tettigonia GZUH CS14062709T Orthoptera KT345954 KT345955 KT375440 KT375441 Wen et al. 2016
Par. yodhathaii TBRC 8502 Coleoptera MH201168 MH188540 MH211354 MH211350 Mongkolsamrit et al. 2019
Pur. lavendulum FMR 10376 Soil FR775489 FR775516 FR775512 Perdomo et al. 2013
Pur. lilacinum CBS 431.87 Tylenchida EF468844 AY624188 EF468791 EF468897 EF468940 Kepler et al. 2012
Pur. takamizusanense NHJ 3582 Hemiptera EU369034 EU369097 EU369015 Johnson et al. 2009
Tolypocladium bacillisporum C53T Eurotiales LC684523 LC684523 LC684523 LC684526 Yamamoto et al. 2022
Tol. cylindrosporum ARSEF 2920T Soil MH871712 MG228381 MG228390 MG228384 MG228387 Vu et al. 2019
Tol. inflatum OSC 71235 Coleoptera EF469077 JN049844 EF469124 EF469061 EF469090 EF469108 Kepler et al. 2012
Tol. ophioglossoides NBRC 106332 Eurotiales JN941409 JN943322 JN941732 JN992466 Schoch et al. 2012
Tol. paradoxum NBRC 100945 JN941410 JN943323 JN941731 AB968599 JN992465 AB968560 Ban et al. 2015
Torrubiellomyces zombiae NY04434801T Hypocreales ON493602 ON493543 ON513396 ON513398 ON513402 Araújo et al. 2022
Polyceph Hypocreales ON513394 Araújo et al. 2022

Abbreviations: ARSEF: Agricultural Research Service Entomopathogenic Fungus Collection, USDA, USA; BBH: BIOTEC Bangkok Herbarium, Thailand; BCC: BIOTEC Culture Collection, Klong Luang, Thailand; BRIP: Queensland Plant Pathology Herbarium, Australia; C: Medical Mycology Research Center, Chiba University, Japan; CBS: Centraalbureau voor Schimmelcultures, Utrecht, the Netherlands; EFCC: Entomopathogenic Fungal Culture Collection, Chuncheon, Korea; FMR: Culture Collection, Facultat de Medicina i Ciències de la Salut, Reus, Spain; GDGM: the Fungal Herbarium of Guangdong Institute of Microbiology, China; GZUH/GACP: Herbarium of Guizhou University, China; GZUIFR: Institute of Fungal Resources of Guizhou University, China; HKAS: Kunming Institute of Botany, Academia Sinica, China; HUA: Herbarium Antioquia University, Medellin, COL; KEW: mycology collection of Royal Botanical Garden, Surrey, UK; NBRC: Biological Resource Center, the National Institute of Technology and Evaluation, Japan; NHJ: Nigel Hywel-Jones personal collection, Thailand; NY: The New York Botanical Garden Herbarium, US; OSC: Oregon State University Herbarium, Corvallis, Oregon, USA; TBRC: Thailand Bioresources Research Center, Thailand; YFCC: Yunnan Fungal Culture Collection of Yunnan University, China; YHH: Yunnan Herbal Herbarium, China.

Sequence alignment and phylogenetic analyses

The taxa used for phylogenetic analyses were selected, based on BLAST search results and related references (Sung et al. 2007; Quandt et al. 2014; Sanjuan et al. 2015; Araújo et al. 2018; Luangsa-Ard et al. 2018). Each locus was independently aligned with the representative sequences using MAFFT v.7 (Katoh and Standley 2013; Katoh et al. 2019). Uninformative gaps and ambiguous regions were removed using Trimal v.1.2 (Capella-Gutiérrez et al. 2009). Trimmed alignments were combined with SequenceMatrix 1.8 (Vaidya et al. 2011). The final combined dataset was deposited on TreeBASE (accession URL: http://purl.org/phylo/treebase/phylows/study/TB2:S30990) and used for Maximum Likelihood analysis and Bayesian analysis. AliView (Larsson 2014) was used to convert format with NEXUS file for Bayesian Inference analysis and FASTA file for Maximum Likelihood analysis. Two strains of Cordyceps militaris (BCC 56302 and YFCC 6587) were selected as outgroup taxa.

Maximum Likelihood (ML) analysis was performed using IQ-TREE 1.6.12 with branch support being estimated from 5000 ultrafast bootstraps (http://iqtree.cibiv.univie.ac.at/, accessed on 04 Sep 2023, Minh et al. (2020)). MrModelTest v. 2.3 (Nylander 2004) as implemented in MrMTgui v.1.0. (Nuin 2007) was used to determine the best-fit evolution model for Bayesian Inference analyses under the Akaike Information Criterion (AIC). The best-fit substitution model GTR+I+G was decided for LSU, ITS, SSU, tef1-α and rpb2 and HKY+I+G for rpb1. MrBayes on XSEDE (3.2.7a) in the CIPRES Science Gateway was utilised to perform Bayesian analysis using Markov Chain Monte Carlo sampling (MCMC). Six simultaneous Markov chains were run for 100,000,000 generations and trees were sampled every 1000 generations. The first 20% of the trees were discarded, as they represented the burn-in phase of the analyses, while the remaining trees were used for calculating posterior probabilities (PP) in the majority rule consensus tree. Bayesian Inference trees convergence was declared when the average standard deviation reached 0.01. The trees were viewed with FigTree v.1.4.0 programme (Rambaut 2016) and edited with Adobe illustrator CS6.

Results

Phylogenetic analyses

Phylogenetic analyses were constructed with combined 6-locus sequences data representing 73 taxa of Ophiocordycipitaceae. The concatenated LSU-ITS-SSU-tef1-α-rpb1-rpb2 data matrix was subjected to Maximum Likelihood (ML) and Bayesian Inference (BI) analyses. Trees were rooted to Cordyceps militaris in Cordycipitaceae. The alignment contains 4831 characters, including gaps (834 bp for LSU, 506 bp for ITS, 1022 bp for SSU, 918 bp for tef1-α, 665 bp for rpb1 and 886 bp for rpb2). The likelihood of the best scoring ML tree was -50301.608. The respective best-fit models determined by ModelFinder on IQ-TREE were GTR+F+I+G4 for LSU, TIM3+F+I+G4 for ITS, K2P+I+G4 for SSU, TIM2+F+I+G4 for TEF1-α, TN+F+I+G4 for RPB1 and RPB2.

In the phylogenetic analyses (Fig. 1), seven genera of Ophiocordycipitaceae are included and their names were labelled on the right side of the tree. The phylogenetic results indicated that the two new species Ophiocordyceps fenggangensis, O. liangii and one new combination O. musicaudata are distinct from other known species. Ophiocordyceps fenggangensis and O. musicaudata form a monophyletic clade close to O. alboperitheciata and Hirsutella kuankuoshuiensis with strong support (100% ML / 1.00 PP, Fig. 1). Ophiocordyceps liangii (HKAS 102546) sister to O. agriotidis with strong support (100% ML/1.00 PP, Fig. 1).

Figure 1. 

Phylogram generated from Maximum Likelihood analysis, based on combined LSU, ITS, SSU, tef1-α, rpb1 and rpb2 sequence data. ML bootstrap values equal to or greater than 95% and the PP equal to or greater than 0.90 are given above each node. The newly-generated sequences are indicated in blue. Type strain, type specimens or neotype are denoted in black bold.

Taxonomy

Ophiocordyceps fenggangensis X. C. Peng & T. C. Wen, sp. nov.

Index Fungorum: IF901112
Facesoffungi Number: FoF14887
Fig. 2

Etymology

Named after the location where the type specimen was found, Fenggang County, Guizhou Province, China.

Figure 2. 

Ophiocordyceps fenggangensis (holotype HKAS 125848) a habitat b host imbedded into the soil with the stroma emerging from the ground c stroma arising from the larva of Lepidoptera d host e, f reverse and front view of the culture on PDA g part of fertile head h part of fertile head with sterile tip (arrow indicate) i perithecia j–m asci n ascus cap o part of ascospores p secondary ascospores. Scale bars: 2 cm (c, e, f); 5 mm (d); 1 mm (g, h); 100 µm (i, j); 25 µm (k–m); 10 µm (n); 5 µm (o); 2 µm (p).

Diagnosis

Parasitic on a larva of Lepidoptera. Stroma arising from the junction between head and thorax of lepidopteran larva, with a sterile tip. Perithecia immersed, grey-white.

Sexual morph

Stroma solitary, unbranched, brown to grey-white, 102 × 1–1.5 mm. Fertile part up to 24 × 1.5 mm, cylindrical, attenuated toward the apex, grey-white when fresh, yellowish when dry, surface spinous due to the protruding ostioles, with a sterile tip (ca. 0.5 mm in length). Stipe cylindrical, brown to black, fibrous, 77.5 × 1–1.2 mm. Perithecia 306–496 × 134–223 μm (x̄= 388.4 × 175.9 µm, σ = 57.35 × 31.05, n = 15), immersed, ovoid to oblong-ovate. Asci 91–176 × 2–8 μm (x̄= 136.5 × 5.3 µm, σ = 38.22 × 2.63, n = 20), cylindrical, hyaline, with thickened apex. Apical cap 2.5–5.0 × 3.5–5.6 μm (x̄= 3.6 × 4.7 µm, σ = 0.78 × 0.48, n = 20), hyaline, hemispherical. Ascospores 0.3–0.7 µm (x̄= 0.4 µm, σ = 38.22 × 2.63, n = 20) wide, filiform, hyaline, easily breaking into part-spores. Secondary ascospores 2.8–6.0 × 0.3–0.7 μm (x̄= 4.0 × 0.4 µm, σ = 0.89 × 0.08, n = 20), cylindrical, smooth-walled. Asexual morph: undetermined.

Culture characteristics

Colonies on PDA, attaining a diameter of 28–32 mm within 39 d at 20 °C, dense, leathery, cream white, convex, undulate margin, reverse brown, radial striation, no sporulation observed.

Material examined

China, Guizhou Province, Fenggang County, Yongan Town (28°05′30.83″N, 107°31′53.38″E, alt. 1149 m), on dead larva of Lepidoptara, 28 April 2021, Xing-Can Peng, FG21042850 (HKAS 125848 holotype, GACP FG21042850 ex-type living culture).

Notes

Multigene phylogenetic analysis showed that Ophiocordyceps fenggangensis forms a sister clade to O. musicaudata with a high support value (98% ML / 0.93 PP) and grouped with O. alboperitheciata and Hirsutella kuankuoshuiensis (Fig. 1). Ophiocordyceps fenggangensis GACP FG21042850 and O. musicaudata GACP SY22072879 have 8 bp differences of nucleotides (0 bp in LSU, 3 bp in tef1-α and 5 bp in rpb1). Morphologically, Ophiocordyceps fenggangensis is distinguished from O. musicaudata in having a solitary unbranched shorter stroma, longer perithecia, smaller asci, narrower ascospores and disarticulating ascospores. Ophiocordyceps alboperitheciata is distinct from O. fenggangensis by its superficial, white to nearly light brown fertile part and ovoid perithecia (Fan et al. 2021), whereas our new species has grey-white to yellowish fertile part and immersed, ovoid to oblong-ovate perithecia. Additionally, the stroma of O. fenggangensis is longer than that of O. alboperitheciata. Perithecia and asci of O. fenggangensis are smaller than those of O. alboperitheciata. Hirsutella kuankuoshuiensis was described only from its asexual morph which is characterised by clavate, narrow fusiform or botuliform conidia; and subulate or slender columnar phialides tapering gradually to a long narrow neck (Qu et al. 2021). BLAST search result showed that the ex-type strain (GACP FG21042850) matches Hirsutella kuankuoshuiensis GZUIFR-2012KKS3-1; however, they are different in 59 bp (including 1 gap) and 8 bp (including 1 gap) within ITS and rpb1 sequences, respectively. The detailed comparisons of the morphologies between these four aforementioned species are shown in Table 2. Based on the morphological differences, we introduce this fungus as a new species of Ophiocordyceps.

Table 2.
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Synopsis of Ophiocordyceps species discussed in the paper.

Species Host Stromata (mm) Perithecia(μm) Asci (μm) Ascospores (μm) Reference
Ophiocordyceps liangii larvae of Lepidoptera 113–188 × 2, paired, cylindrical, unbranched, brown to dark brown 350–548 × 203.5–446, superficial, brown, obovoid 122–271.5 × 3.5–13.5, filiform, 8-spored, with thickened apices 67.5–270.5 × 1.5–4.0, filiform to spindle, non-disarticulating This study
Ophiocordyceps agriotidis larvae of Elateridae, Coleoptera 70 × 1, solitary, cylindrical, black brown to black 400–480 × 225–300, superficial to pseu-immersed, ovoid 235–300 × 12, cylindrical, with an oblate apical cap 115–150 × 4.2–45, cylindricial, multi-septate, non-disarticulating Liang (2007)
Ophiocordyceps brunneiperitheciata Lepidopteran larvae 4–8 × 0.5–1, paired to multiple, simple, wiry to pliant or fibrous 350–400 × 180–200, superficial, brown to dark brown, ovoid 125–175 × 6–8, cylindrical, 8-spored, with thickened apices 110–160 × 3–4, filiform, multi-septate, non-disarticulating Luangsa-Ard et al. (2018)
Ophiocordyceps fenggangensis larvae of Lepidoptera 102 × 1–1.5, solitary, cylindrical, brown to off-white 306–496 × 134–223, immersed, off-white to yellowish, ovoid to oblong-ovate. 91–176 × 2–8, cylindrical, apex thickened 0.3–0.7 wide, filiform, hyaline, disarticulating, secondary ascospores 2.8–6.0 × 0.3–0.7, cylindrical This study
Ophiocordyceps alboperitheciata larva of Noctuidae, Lepidoptera 69–71 × 0.6–1.2, paired, cylindrical, unbranched, with a sterile tip, light brown to dark brown 410–550 × 230–320, superficial, white to pale brown, nearly ovoid 144–246 × 3.5–4.7, cylindrical, 8-spored, with a hemispheric apical cap 0.5–0.6 wide, multi-septate, non-disarticulating Fan et al. (2021)
Ophiocordyceps musicaudata larvae of Lasiocampidae, Lepidoptera 130–140 × 1–2, solitary or numerous, simple or branched, cylindrical, brown to yellowish 260–492 × 144–314, immersed, yellowish, flask-shaped. 123–264 × 5–13, filiform, cylindrical, 8-spored, usually without thickened apices 114–298 × 1.5–4.0, cylindrical, irregular multi-septate, non-disarticulating This study
Ophiocordyceps musicaudata larvae of Lasiocampidae, Lepidoptera up to 165 in length, twin, unbranched, light brown to white 420 × 210, immersed, pseudo-oval 230 × 7.6, cylindrical, with short cylindrical apices filiform, multi-septate Liang et al. (1996)
Ophiocordyceps larvarum larva of Lepidoptera 90 × 3.5, solitary, cylindrical, cinnamon light brown 340–380 × 160–200, pseudo-embedding, oblong 180–200 × 8.5, with a hemispheric ascus cap 4-9 × 2-2.5, columnar, septate Liang et al. (2007)
Cordyceps ochraceostromata larva of Lepidoptera up to 60 in length, single or paired, cylindrical, pale ochraceous-reddish to brownish 350 × 200, immersed, ovoid up to 7 in width, with thickened apices disarticulating, secondary ascospores 7–10 × 1.5–2, truncated on both sides Kobayasi and Shimizu (1980)
Ophiocordyceps zhangjiajiensis pupa of Lepidoptera 100 × 2, single or paired, cylindrical, not ramified, leathery, brown to snuff-coloured 330–375 × 180–230, pseudo-embedding, ovoid 200 × 10, approximately fusiform, with thickened apices disarticulating, secondary ascospores 15–23 × 3, cylindrical Liang et al. (2002)
Ophiocordyceps dayiensis larva of Lepidoptera 140 × 2, single, filiform, unbranched, brownish 430–480 × 210–270, immersed, narrowly ovoid 225–345 × 6–7.5, slender cylindric, with very thin cap of ascus 300 × 1–1.8, filiform, multi-septate, non-disarticulating Liang et al. (2003)
Ophiocordyceps emeiensis larva of Hepialidae, Lepidoptera 100–160 × 1.5–3, single or paired, branched, brown 320–460 × 220–320, superficial, brown to black, ellipsoid or ovoid 173–213 × 7.5–8, cylindrical, with hemisphacris heads 45–60 × 1–1.5, filiform, multi-septate Liang et al. (2007)
Ophiocordyceps laojunshanensis Larvae of Hepialidae, Lepidoptera 47–93 × 1–3.9, simple, rarely 2 or 3, apex sterile acuminate, purplish to dark brown 200–300 × 200–350, globoid, arranged loosely in irregular lateral cushions. 165–275 × 11.5–14.5, clavate 130.0–250 × 5–6, filiform, septate Chen et al. (2011)
Ophiocordyceps paludosa larvae of Lepidoptera 55–130 × 0.5–1.0, slender filiform, greyish-brown 800–855 × 375–410, superficial, greyish-brown to deep brown, flattened-ovoid 480–550 × 8–10, cylindrical 390–490 × 2.0–2.5, filiform, multi-septate, non-disarticulating Mains (1940)

Ophiocordyceps liangii X. C. Peng & T. C. Wen, sp. nov.

Index Fungorum: IF901113
Facesoffungi Number: FoF14888 Fig. 3

Etymology

Named in honour of Prof. Zong-Qi Liang, who has made a significant contribution to the studies of Cordyceps sensu lato.

Figure 3. 

Ophiocordyceps liangii (holotype HKAS 125845) a habitat b, c stromata arising from host d superficial perithecia e host f, g section of perithecia h–k asci h–i immature j, k mature l, m ascus cap n–p ascospores q–s reverse and front view of culture on PDA. Scale bars: 4 cm (b, c), 1 mm (d), 5 mm (e), 100 µm (f, g), 50 µm (h–k), 20 µm (l, m), 30 µm (n–p), 2 cm (q–s).

Diagnosis

Parasitic on lepidoptaran larva. Stroma arising from the back and tail of host, no sterile tip. Perithecia superficial, dark brown.

Sexual morph

Stroma paired, flexuous, fibrous, filiform, tapering gradually towards the apex, unbranched, brown to dark brown, 11.3–18.8 × 0.2 cm. Fertile part cylindrical, dark brown, 5.4–6.1 × 0.2 cm. Stipe flexuous, brown, 5.1–13.5 × 0.1–0.2 cm. Perithecia 350–548 × 203.5–446 μm (x̄= 430.5 × 296 µm, σ = 56.45 × 60.83, n = 25), superficial, brown, obovoid. Asci 122–271.5 × 3.5–13.5 μm (x̄= 204.8 × 8.0 µm, σ = 38.22 × 2.63, n = 40), filiform, 8-spored, cylindrical, with thickened apices. Apical cap 1.7–4.5 × 4.0–6.6 μm (x̄= 3.2 × 5.4 µm, σ = 0.56 × 0.59, n = 40), hyaline, conspicuous. Ascospores 67.5–270.5 × 1.5–4.0 µm (x̄= 151.3 × 2.6 µm, σ = 36.31 × 0.61, n = 55), fusiform to filiform, aseptate, guttulate, non-disarticulating. Asexual morph: undetermined.

Culture characters

Colonies on PDA, attaining a diameter of 21–27 mm within 25 d at 25 °C, dense, leathery, pale yellow at centre, white at periphery, radially striate, with brown or translucent droplets, reverse black brown, producing brown pigment. Sporulation not observed.

Material examined

China, Guizhou Province, Libo County, Xiaoqikong Scenic Area (25°15′15.68″N, 107°43′43.98″E, alt. 458 m), on dead larva of Lepidoptara, on leaf litter, 12 July 2022, Xing-Can Peng, LB22071253 (HKAS 125845 holotype, GACP LB22071253 ex-type culture).

Notes

Phylogenetic analyses revealed that Ophiocordyceps liangii is closely related to O. agriotidis and O. brunneiperitheciata with high support (100% ML/1.00 PP, Fig. 1). Ophiocordyceps liangii differs from O. brunneiperitheciata and O. agriotidis in having longer stroma, larger perithecia and asci (see Table 2). The comparison of the nucleotide sequences between O. liangii (GACP LB22071253) and O. brunneiperitheciata (TBRC 8100) showed 23 bp (including 3 gaps) differences in LSU, 102 bp in tef1-α and 88 bp in rpb2 sequences. Ophiocordyceps liangii differs from O. agriotidis ARSEF 5692 by 3 bp in SSU, 70 bp (including 20 gaps) in ITS, 20 bp (including 1 gap) in LSU, 106 bp in tef1-α and 79 bp in rpb2. Henceforth, we describe this taxon as a new species in Ophiocordyceps.

Ophiocordyceps musicaudata (Z. Q. Liang & A. Y. Liu) X. C. Peng & T. C. Wen, comb. nov.

Index Fungorum: IF901114
Facesoffungi Number: FoF14889
Fig. 4

Cordyceps musicaudata Z. Q. Liang & A. Y. Liu. Basionym.

Diagnosis

Parasitic on larvae of insect (Lasiocampidae, Lepidoptera). Stroma arising from body of the host, no sterile tip. Perithecia immersed, yellowish.

Figure 4. 

Ophiocordyceps musicaudata (HKAS 131911) a redrawn of Liang (2007) b habitat c, d stromata arising from host e fertile parts f, g reverse and front view of culture on PDA h, i perithecia j–l asci m ascus cap n–p ascospores, the arrows in the n, p indicating septate. Scale bars: 2 cm (c, d); 5 mm (e); 1 cm (f, g); 100 µm (h, i); 50 µm (j–l, n–p); 5 um (m).

Sexual morph

Stroma solitary, paired to multiple, simple or branched, flexuous, cylindrical with acute or round ends, 13–14 × 0.1–0.2 cm. Fertile part cylindrical, yellowish, 2–4.3 × 0.1–0.2 cm. Stipe flexuous, brown, 10–12 × 0.1 cm. Peridium 15–49 µm (x̄= 33 µm, σ = 8.41, n = 40) wide, composed of brown cells of textura angularis. Perithecia 260–492 × 144–314 μm (x̄= 378 × 221 µm, σ = 37.29 × 1.57, n = 25), immersed, flask-shaped. Asci 123–264 × 5–13 μm (x̄= 191 × 8.1 µm, σ = 58.76 × 48.94, n = 80), cylindrical, 8-spored, with inconspicuous thickened cap. Ascospores 114–298 × 1.5–4.0 µm (x̄= 198 × 2.3 µm, σ = 46.03 × 0.48, n = 45), filiform, irregular multi-septate, non-disarticulating. Asexual morph: undetermined.

Culture characteristics

Colonies on PDA, attaining a diameter of 21–27 mm within 43 d at 25 °C, dense, velvety, off-white, wrinkled bulge, reverse brown. No sporulation observed.

Epitype designated here

China, Guizhou Province, Suiyang County, Kuankuoshui National Nature Reserve (28°13′N, 107°09′E, alt. 1470–1507 m), on dead larva of Lepidoptera sp. buried in soil, 28 July 2022, Xing-Can Peng, SY22072880 (HKAS 131911 epitype); Ting-Chi Wen, SY22072879 (HKAS 131912, GACP SY22072879, live culture).

Notes

Liang et al. (1996) published a new species, Cordyceps musicaudata solely based on morphological observation. The type specimen (CGAC89-62301) was found on the insect (Lasiocampidae, Lepidoptera) in the Kuankuoshui National Nature Reserve, Guizhou Province, China. It is regrettable that the type specimen has been destroyed, thus its DNA and morphological observations could not be obtained. Liang et al. (1996) stated that the type specimen has characteristics of paired rat-tailed stromata, white to pale brown fertile part, brown stipe, immersed perithecia, cylindrical asci with thickened apices and filiform, multi-septate ascospores. In this study, we collected two fresh specimens from the same location to the type specimen. The fresh specimen shares similar morphology with the type specimen of C. musicaudata in the lepidopteran hosts, stipitate rat-tailed stromata with yellowish fertile part, immersed perithecia and filiform, multi-septate, intact ascospores. Phylogenetic analysis indicated that C. musicaudata has close affinity with O. alboperitheciata and O. fenggangensis with adequate support (99% ML / 1 PP, Fig. 1). The differences between C. musicaudata and O. fenggangensis have been mentioned in the notes of O. fenggangensis. The difference between C. musicaudata and O. alboperitheciata is the size and the arrangements of the perithecia. Ophiocordyceps musicaudata has smaller and immersed perithecia, whereas O. alboperitheciata has larger and superficial perithecia. The detailed comparisons of morphologies between our specimen and related species including species without molecular data are shown in Table 2 (Cordyceps ochraceostromata, Ophiocordyceps alboperitheciata, O. dayiensis, O. emeiensis, O. fenggangensis, O. laojunshanensis, O. larvarum, O. zhangjiajiensis and O. paludosa). Our specimen morphologically more matches Cordyceps musicaudata rather than other Ophiocordyceps species included in the Table 2. Therefore, we determined these specimens as Cordyceps musicaudata and move this species into the genus Ophiocordyceps, based on the phylogenetic affiliation of this new collection.

Discussion

It has been observed that there are eight genera in Ophiocordycipitaceae that possess versatile lifestyles (Crous et al. 2020; Araújo et al. 2022; Xiao et al. 2023). Drechmeria typically live as endoparasites inside nematodes and lepidopteran larvae (Yu et al. 2018). Hantamomyces is a monotypic genus that was established by Crous et al. (2020), based on H. aloidendri found on the leaves of Aloidendron dichotomum. Most species of Harposporium parasitise free-living nematodes and rotifers; however, the taxonomic status of some species in this genus is still difficult to determine (Crous et al. 2023). Paraisaria accommodate 18 species that were established due to their distinctive features, such as the fleshy, robust solitary stroma, globose to ovoid fertile head and brighter colour. These characteristics are different from other Ophiocordycipitaceae species (Mongkolsamrit et al. 2019). Purpureocillium contains six species that are entomopathogenic fungi> or pathogenic to humans (Luangsa-Ard et al. 2011). Species of Tolypocladium infect hosts crossing animals, plants and fungi>, showing highly diverse lifestyles (Yu et al. 2021). Torrubiellomyces is a genus with only one species that is a mycoparasite. The species has superficial perithecia that grow directly on the host’s surface (Araújo et al. 2022). Genera of Ophiocordycipitaceae are monophyletic with the exception of Ophiocordyceps which has been split into three clades due to erection of Paraisaria (Mongkolsamrit et al. 2019; Wei et al. 2021b; Wei et al. 2022). So far, there are 419 species in the Ophiocordyceps, including 98 unclarified Hirsutella species (until 28 Aug 2023). Amongst them, molecular data are not available for 194 species. In this study, 75 taxa representing 70 species of Ophiocordyceps are sampled and used for phylogenetic analysis. The topologies of the main clades are similar to previous studies (Wei et al. 2022; Xiao et al. 2023). Insertion of Paraisaria causes paraphyly of Ophiocordyceps; Drechmeria and Purpureocillium form a clade sister and Harposporium forms a clade sister with Ophiocordyceps s. s. and Paraisaria (Xiao et al. 2023). The sexual morphs of Ophiocordyceps species phenotypically share a darkly or brightly coloured, fibrous stromata often with aperithecial apices or lateral pads. Perithecia are superficial to completely immersed, ordinal or oblique in arrangement. Asci are cylindrical to filiform with thickened apex. Ascospores are cylindrical, multi-septate, disarticulating into secondary spores or not (Sung et al. 2007). However, they can be distinguished according to their associated host, arrangement of perithecia, size, shape, colour of fertile part and morphologies of ascospores and part-spores. Notably, combined molecular phylogenetic analysis provides further evidence of their interspecific relationship.

Most of the fungal species published before the 1990s relied on classical morphology to determine the taxonomic status. It is difficult to gain access to their molecular data and morphological illustration and other related information as well as their type specimens. These issues emphasise the importance of collecting fresh specimens and clarifying them with modern approaches. Such work has been conducted by Sung et al. (2007) who systematically classified Cordyceps and clavicipitaceous fungi> through molecular phylogenetic analysis and revised most of the species of Cordyceps s. l. Henceforth, an increasing number of new species were described and the natural classification of hypocrealean entomopathogens were gradually elucidated, based on more sufficient taxa sampling (Ban et al. 2009; Evans et al. 2011; Sanjuan et al. 2015; Simmons et al. 2015; Spatafora et al. 2015; Araújo et al. 2018; Khonsanit et al. 2019; Araújo et al. 2020; Mongkolsamrit et al. 2021; Yang et al. 2021; Araújo et al. 2022; Mongkolsamrit et al. 2022; Tang et al. 2022; Mongkolsamrit et al. 2023; Tang et al. 2023a, b). However, Cordyceps musicaudata has not been revised because there are no specimens available for study of its morphological and molecular data. We have conducted a study wherein fresh specimens were collected from the same location as the type of Cordyceps musicaudata. Our observations reveal that there are certain similarities between the fresh specimen and some species mentioned in Table 2, both at a macroscopic and microscopic level. However, we also observed noticeable differences between them. For example, the perithecia of Ophiocordyceps larvarum and O. zhangjiajiensis are pseudo-immersed; O. emeiensis and O. paludosa have superficial perithecia; the ascospores of O. dayiensis are slender; the stromata of O. laojunshanensis are short and the perithecia are globoid; and the ascospores of Cordyceps ochraceostromata disarticulate into secondary spores (see Table 2). Based on molecular analysis and updated morphological illustration, we identified the specimen as Cordyceps musicaudata and synonymised it as O. musicaudata. Moreover, two new species, O. fenggangensis and O. liangii are described from their sexual morphs and phylogenetic results support their novelty.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

This study was supported by the Science and Technology Foundation of Guizhou Province (No. [2022]025-8, No. GZU-SZBJMS001 & No. (2020-1Y391)).

Author contributions

Investigation: YW, GYW. Resources: YZ, XZ, YHL. Writing – original draft: TCW, XCP. Writing – review and editing: DPW, JDL, KT.

Author ORCIDs

Xing-Can Peng https://orcid.org/0000-0002-7271-7639

Ting-Chi Wen https://orcid.org/0000-0003-1744-5869

De-Ping Wei https://orcid.org/0000-0002-3740-0142

Yi Wang https://orcid.org/0009-0006-5412-7893

Xian Zhang https://orcid.org/0009-0008-0919-4303

Khanobporn Tangtrakulwanich https://orcid.org/0009-0002-7081-618X

Jian-Dong Liang https://orcid.org/0000-0002-3939-3900

Data availability

All of the data that support the findings of this study are available in the main text.

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