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Research Article
Morphology and multigene phylogeny reveal three new species of Samsoniella (Cordycipitaceae, Hypocreales) from spiders in China
expand article infoTing Wang‡§, Jun Li‡, Xiaoyun Chang‡, Zengzhi Li|‡, Nigel L. Hywel-Jones|, Bo Huang‡, Mingjun Chen‡
‡ Anhui Agricultural University, Hefei, China
§ Natural Resources and Planning Bureau of Bengbu City, Bengbu, China
| Zhejiang BioAsia Institute of Life Sciences, Pinghu, China

Corresponding author: Bo Huang ( bhuang@ahau.edu.cn )

Corresponding author: Mingjun Chen ( mjchen@ahau.edu.cn )

Academic editor: Sajeewa Maharachchikumbura
© 2024 Ting Wang, Jun Li, Xiaoyun Chang, Zengzhi Li, Nigel L. Hywel-Jones, Bo Huang, Mingjun Chen.
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: Wang T, Li J, Chang X, Li Z, Hywel-Jones NL, Huang B, Chen M (2024) Morphology and multigene phylogeny reveal three new species of Samsoniella (Cordycipitaceae, Hypocreales) from spiders in China. MycoKeys 101: 329-346. https://doi.org/10.3897/mycokeys.101.111882
Open Access

Abstract

The genus Samsoniella was erected based on orange cylindrical to clavate stromata, superficial perithecia and conidiophores with Isaria-like phialides and to segregate them from the Akanthomyces group. In this study, based on morphological features and multigene (SSU, LSU, TEF, RPB1 and RPB2) phylogenetic analysis six Samsoniella species parasitizing spiders were collected in China. Three of them belong to known species S. alpina, S. erucae and S. hepiali. Three new species S. anhuiensis sp. nov., S. aranea sp. nov. and S. fusiformispora sp. nov. are illustrated and described. They are clearly distinct from other species in Samsoniella occurring in independent subclades. Furthermore, among the four insect-pathogenic fungi specimens collected from similar sites, three of them were identified as the new species described below. Our study significantly broadens the host range of Samsoniella from Insecta to Arachnida, marking a noteworthy expansion in understanding the ecological associations of these fungi. Additionally, the identification of both mononematous and synnematous conidiophores in our study not only expands the knowledge of Samsoniella species but also provides a basis for future research by comparing the ecological significance between these conidiophore types. In conclusion, our study enhances the understanding of Samsoniella diversity, presenting a refined phylogenetic framework and shedding light on the ecological roles of these fungi in spider parasitism.

Key words

Araneogenous fungi, Isaria-like, Samsoniella, taxonomy

Introduction

The genus Isaria Pers. was established by Persoon (1794) with I. farinosa (Pers.) Fr. as the type species (Hodge et al. 2005). Isaria is characterized by the formation of branched synnemata that give rise to flask-shaped phialides produced in whorls. For a considerable period, Isaria has been considered the asexual morph of Cordyceps sensu stricto, a classification within the family Cordycipitaceae, which encompasses numerous species featuring pallid or brightly pigmented, fleshy stromata (Sung et al. 2007; Maharachchikumbura et al. 2015). Samson (1974) transferred some species including I. farinosa to Paecilomyces Bainer (1907). However, Hodge et al. (2005), based on morphological and molecular phylogenetic studies, moved Paecilomyces farinosa back to Isaria re-establishing the type as Isaria farinosa (Holmsk.) Fr. Most of the insect-pathogenic mesophilic Paecilomyces species in sect. Isarioidea of Samson (1974) were transferred to Isaria (Luangsa-ard et al. 2004, 2005; Gams et al. 2005). Nonetheless, Kepler et al. (2017) proposed the rejection of the genus Isaria due to the polyphyletic distribution of Isaria species. Recently, molecular phylogenetic analysis, has shown that some Isaria-like fungi are distributed in the genus Akanthomyces of the family Cordycipitaceae, forming monophyletic branches and are closely related to the genus Akanthomyces. Mongkolsamrit et al. (2018) established this phylogenetic branch as a new genus Samsoniella Mongkols., Noisrip., Thanakitp., Spatafora & Luangsa-ard. They accommodated three species of Lepidoptera entomopathogenic fungi in the genus; S. alboaurantia (G. Sm.) Mongkolsamrit, S. aurantia Mongkolsamrit and S. inthanonensis Mongkolsamrit. The three species have orange cylindrical to clavate stromata, superficial perithecia and orange conidiophores with Isaria-like phialides and hyaline conidia.

Over the past seven years, there has been extensive research on the species diversity within the genus Samsoniella, possibly driven by the significant medical and ecological value associated with certain species in the genus. In a follow-up study, Wang et al. (2020a) documented nine new species within the genus Samsoniella. Specifically, Paecilomyces hepiali Chen, formerly misconstrued as the asexual counterpart of Ophiocordyceps sinensis, demonstrated the ability to produce Isaria-like phialides. The perplexing taxonomic status of P. hepiali prompted taxonomists to reconsider its classification. Wang et al. (2020a) determined that the most suitable systematic position for P. hepiali is within the genus Samsoniella. Consequently, they proposed the new taxonomic combination S. hepiali for this species. Subsequently, Chen et al. (2020) described three additional species of Samsoniella. Furthermore, phylogenetic analysis led to the repositioning of strains previously identified as I. farinosa. Notably, strains CBS 240.32 and CBS 262.58 were integrated into the genus Samsoniella and redesignated as S. alboaurantia (Mongkolsamrit et al. 2018; Chen et al. 2021). Similarly, strains OSC 111005 and OSC 111006 were reassigned to S. farinosa Wang (Wang et al. 2020b). More recently, Chen et al. (2021, 2022, 2023), Wang et al. (2022), Wang et al. (2023) and Crous et al. (2023) contributed descriptions of fifteen additional novel Samsoniella species. Consequently, the genus Samsoniella now comprises a total of thirty-one recognized species.

We carried out a series of surveys for spider pathogenic fungi in China. A total of seven spider cadavers infected by Samsoniella were collected and isolated. Based on morphological and molecular phylogenetic analyses, three were identified as S. alpina, S. erucae, and S. hepiali. However, the other four strains represented four new species, which are described here as S. anhuiensis sp. nov., S. aranea sp. nov. and S. fusiformispora sp. nov. Among the four insect-pathogenic fungi specimens collected from the same sites, three of them were identified as the new species described below. Our study enhances the understanding of Samsoniella diversity, presenting a refined phylogenetic framework and shedding light on the ecological roles of these fungi in spider parasitism.

Materials and methods

Sample collection, isolation and morphological observations

The majority of spider specimens infected by fungi were collected from all over China. Four specimens were collected from the Jingting Mountains National Forest Park, Anhui Province, southeastern China. Four specimens were collected from the Jinggang Mountains National Nature Reserve, Jiangxi Province, southeastern China. One specimen was collected from the Maiji National Forest Park, Gansu Province, northwestern China. One specimen was collected from the Yaoluoping National Forest Park, Anhui Province, southeastern China, and one specimen was collected from the Wanfo Mountains, Anhui Province, southeastern China. Several insect specimens infected by fungi were collected from sites similar to those where spider specimens were collected. The collections were noted and photographed in the field, then carefully deposited in plastic boxes and returned to the laboratory. Fungal cultures were isolated from fresh conidia or mycelia from spider cadavers. Pure cultures were established and incubated on fresh potato dextrose agar (PDA) plates and grown at 25 °C for 2 weeks. The fresh structures of specimens and isolated strains were mounted in water for measurements and lactophenol cotton blue solution for microphotography following Wang et al. (2020a). Features such as size and shape of conidia, colony color in culture, were made from squash mounts and sections made from fresh specimen and culture grown on oatmeal agar (OA, Difco), PDA and one quarter strength SDAY (SDAY/4, Difco) (Bischoff et al. 2009). The color of the cultures was characterized using the Naturalist’s Color Guide (Smith 1975). Microscopic observations were made from squash mounts and sections made from fresh material using a ZEISS Axiolab 5 microscope. All samples and strains studied here were deposited in the Research Center for Entomogenous Fungi (RCEF) of Anhui Agricultural University.

DNA extraction, PCR amplification and sequencing

Total genomic DNA was extracted from cultured mycelia with CTAB method (Liu et al. 2001), then stored in -20 °C. Two gene regions, namely the small subunit ribosomal RNA (SSU) and large subunit ribosomal RNA (LSU) were sequenced from the cell nuclei, and three protein coding genes, translation elongation factor-1a (TEF) and the largest and second largest subunits of RNA polymerase II (RPB1 and RPB2) were used in this study. The SSU and LSU were amplified with NS1/NS4 (White et al. 1990) and LROR (Vilgalys and Hester 1990)/LR7(Hopple 1994). The TEF with 983F/2218R (Rehner and Buckley 2005), RPB1 with CRPB1/RPB1–Cr (Castlebury et al. 2004) and RPB2 with fRPB2–7CR /fRPB2–5F (Liu et al. 1999) were amplified. PCR reactions of the five nuclear loci were carried out in 25 μL reaction mixture containing 12.5 μL 2× Taq Plus MasterMix (CoWin Biosciences, Beijing, China), 1 μL of each primer (10 μM), 1.5 μL of template DNA (1–2 ng) and 9 μL of sterile water. PCR cycle conditions were as previously described (Sung et al. 2007). PCR products were purified and sequenced by Sangon Company (Shanghai, China). The resulting sequences were checked manually, then submitted to GenBank.

Sequence alignment and phylogenetic analyses

The sequences in this study were uploaded to BLAST and searched in the GenBank database to determine probable taxa. DNA sequences generated in this study were assembled and edited using version 6.0. DNASTAR. Generated SSU, LSU, TEF, RPB1 and RPB2 sequences were aligned with those published by Chen et al. (2020) and Wang et al. (2020a) and others downloaded from GenBank were used as a dataset of taxa in Samsoniella and closely related Samsoniella groups (Table 1). Sequences of the genus Akanthomyces (A. aculeatus HUA772 and HUA 186145) were chosen as the outgroup. Multiple sequence alignment was conducted with MAFFT 7.3.13 (Katoh and Standley 2013). The final sequence alignment of the combined dataset was used for analyses using Maximum Likelihood (ML) and Bayesian Inference (BI) to infer their phylogenetic relationships.

Table 1.
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Species, strain numbers, accession numbers and origins of Samsoniella and related taxa used in this study, new sequences were shown in bold.

Species Strain No. GenBank accession No.
SSU LSU TEF RPB1 RPB2
Akanthomyces aculeatus HUA772 KC519368 KC519370 – – –
A. aculeatus HUA186145T MF416572 MF416520 MF416465 – –
A. cf. coccidioperitheciatus NHJ 5112 EU369109 EU369043 EU369026 EU369066 –
A. coccidioperitheciatus NHJ 6709 EU369110 EU369042 EU369025 EU369067 EU369086
A. farinosa CBS541.81 MF416606 MF416553 – MF416655 –
A. lecanii CBS101247 AF339604 AF339555 DQ522359 DQ522407 DQ522466
A. muscarius CBS 143.62 KM283774 KM283798 KM283821 KM283841 KM283863
Beauveria bassiana ARSEF1564T – – HQ880974 HQ880833 HQ880905
B. brongniartii ARSEF 617T – – HQ880991 HQ880854 HQ880926
BCC 16585 – JF415967 JF416009 JN049885 JF415991
B. staphylinidicola ARSEF 5718 EF468981 EF468836 EF468776 EF468881 –
Cordyceps farinosa CBS111113 AY526474 MF416554 GQ250022 MF416656 GU979973
C. militaris OSC 93623 AY184977 AY184966 DQ522332 DQ522377 AY545732
Isaria sp. spat 09-050 MF416613 MF416559 MF416506 MF416663 MF416457
spat 09-051 MF416614 MF416560 MF416507 MF416664 MF416458
Samsoniella alboaurantium CBS 240.32 JF415958 JF415979 JF416019 JN049895 JF415999
CBS 262.58 – – MF416497 MF416654 MF416448
S. alpina YFCC 5818 MN576753 MN576809 MN576979 MN576869 MN576923
YFCC 5831 MN576754 MN576810 MN576980 MN576870 MN576924
S. alpina RCEF0643 – – OM482385 – –
S. anhuiensis RCEF2830 OM268843 OM268848 OM483864 OM751889 –
RCEF2590 OR978313 OR978316 OR966516 OR989964 –
S. antleroides YFCC 6016 MN576747 MN576803 MN576973 MN576863 MN576917
YFCC 6113 MN576748 MN576804 MN576974 MN576864 MN576918
S. aranea RCEF2831 OM268844 OM268849 OM483865 OM751882 OM802500
RCEF2868 OM268845 OM268850 OM483866 OM751883 OM802501
RCEF2870 OR978314 OR978317 OR966517 OR989965 OR989966
S. aurantia TBRC 7271T – MF140728 MF140846 MF140791 MF140818
TBRC 7273 – – MF140844 – MF140816
S. cardinalis YFCC5830 MN576732 MN576788 MN576958 MN576848 MN576902
YFCC 6144 MN576730 MN576786 MN576956 MN576846 MN576900
S. cristata YFCC6021 MN576735 MN576791 MN576961 MN576851 MN576905
YFCC6023 MN576736 MN576792 MN576962 MN576852 MN576906
S. coccinellidicola YFCC8772 ON563166 ON621670 ON676514 ON676502 ON568685
YFCC8773 ON563167 ON621671 ON676515 ON676503 ON568686
S. coleopterorum A19502 – – MT642602 MT642603 MN101587
S. duyunensis DY09162 – OQ363114 OQ398146 – –
DY07501 – OR263307 OR282780 OR282773 OR282776
DY07502 – OR263427 OR282781 – OR282777
S. erucae KY11121 – ON502835 ON525425 – ON525424
KY11122 – ON502822 ON525427 – ON525426
S. erucae RCEF2595 OM268842 OM268847 OM483863 OM751888 –
RCEF2592 – – OR966518 – –
S. farinosa OSC111005 DQ522558 DQ518773 DQ522348 DQ522394 –
OSC111006 EF469127 EF469080 EF469065 EF469094 –
S. farinospora YFCC8774 ON563168 ON621672 ON676516 ON676504 ON568687
YFCC9051 ON563169 ON621673 ON676517 ON676505 ON568688
S. fusiformispora RCEF5406 OM268846 OM268851 OM483867 OM751890 –
RCEF2588 OR978312 OR978315 OR966515 – –
S. guizhouensis KY11161 – ON502830 ON525429 – ON525428
KY11162 – ON502846 ON525431 – ON525430
S. haniana YFCC8769 ON563170 ON621674 ON676518 ON676506 ON568689
YFCC8770 ON563171 ON621675 ON676519 ON676507 ON568690
YFCC8771 ON563172 ON621676 ON676520 ON676508 ON568691
S. hepiali YFCC 5823 MN576745 MN576801 MN576971 MN576861 MN576915
YFCC 5828 MN576744 MN576800 MN576970 MN576860 MN576914
S. hepiali RCEF1481 OL854202 – OM482386 – –
S. hymenopterorum A19521 – – MN101588 MT642603 MT642604
A19522 – – MN101591 MN101589 MN101590
S. inthanonensis TBRC 7915 – MF140725 MF140849 MF140790 MF140815
S. kunmingensis YHH16002 MN576746 MN576802 MN576972 MN576862 MN576916
S. lanmaoa YFCC6148T MN576733 MN576789 MN576959 MN576849 MN576903
YFCC6193 MN576734 MN576790 MN576960 MN576850 MN576904
S. lepidopterorum DL10071 – – MN101594 MN101592 MN101593
DL10072 – – MT642606 – MT642605
S. neopupicola KY11321 – ON502839 ON525433 – ON525432
KY11322 – ON502833 ON525435 – ON525434
S. pseudogunnii GY407201 – MZ827010 – – –
GY407202 – MZ831865 – – –
S. pseudotortricidae YFCC9052 ON563173 ON621677 ON676521 ON676509 ON568692
YFCC9053 ON563174 ON621678 ON676522 ON676510 ON568693
S. pupicola DY101681 – MZ827009 MZ855231 – MZ855237
DY101682 – MZ827635 MZ855232 – MZ855238
S. ramosa YFCC6020T MN576749 MN576805 MN576975 MN576865 MN576919
S. sinensis YFCC8766 ON563175 ON621679 ON676523 ON676511 ON568694
YFCC8767 ON563176 ON621680 ON676524 ON676512 ON568695
YFCC8768 ON563177 ON621681 ON676525 ON676513 ON568696
S. tiankengensis KY11741 – ON502838 ON525437 – ON525436
KY11742 – ON502841 ON525439 – ON525438
S. tortricidae YFCC6013 MN576751 MN576807 MN576977 MN576867 MN576921
YFCC6131 MN576750 MN576806 MN576976 MN576866 MN576920
S. vallis DY07241 – OR263306 OR282778 OR282772 OR282774
DY07242 – OR263308 OR282779 – OR282775
DY091091 – OR263428 OR282782 – –
DY091092 – OR263431 OR282783 – –
S. winandae TBRC17511 – OM491231 OM687896 OM687901 OM687899
S. winande TBRC17512 – OM491232 OM687897 OM687902 OM687900
S. yunnanensis YFCC 1527 MN576756 MN576812 MN576982 MN576872 MN576926
YFCC 1824 MN576757 MN576813 MN576983 MN576873 MN576927

Boldface: data generated in this study.

Phylogenetic inference was done according to Maximum Likelihood (ML) using RAxML version 8 (Stamatakis 2014) and Bayesian Inference (BI) using MrBayes v.3.2 (Ronquist et al. 2012). For the ML analysis, we used the GTRCAT model for all partitions, in accordance with recommendations in the RAxML manual against the use of invariant sites and 1000 rapid bootstrap replicates. The GTR+I+G model was selected by MrModeltest 2.2 (Darriba et al. 2012) as the best nucleotide substitution model for the Bayesian analysis. Four MCMC chains were executed simultaneously for 2000,000 generations, sampling every 100 generations. Finally, phylogenetic trees were visualized using the Interactive Tree of Life (iTOL) (https://itol.embl.de) online tool (Letunic and Bork 2016).

Results

Phylogenetic analysis

To determine the phylogenetic relationship between these fungi and allied species from NCBI we constructed a phylogenetic tree based on Maximum Likelihood (ML) and Bayesian analysis, based on concatenated sequences of five genes included 89 taxa, comprising 4491 characters (SSU: 1047bp, LSU: 849 bp, TEF: 945bp, RPB1: 717 bp, RPB2: 933bp). The multi-gene phylogenetic tree consisted of four genera belonging to the family Cordycipitaceae, including Akanthomyces, Beauveria, Cordyceps and Samsoniella, with strong support (100%). Statistical support (≥75%/0.75) is shown at the nodes for ML bootstrap support/BI posterior probabilities and the strains’ numbers are noted after each species’ name (Fig. 1).

Figure 1. 

Phylogenetic relationships between the genus Samsoniella and closely-related species, based on multigene dataset (SSU, LSU, TEF, RPB1 and RPB2) for maximum likelihood/ Bayesian method. Note: The ML tree presented here, and the node support rate of the two methods is displayed on the branches. The maximum likelihood support values /Bayesian posterior probabilities value (≥75%/0.75) are shown, and bold lines mean support for the two analyses were 98%. The typical strain of the species is marked with the superscript “T”

In the phylogenetic tree, Samsoniella species clustered in a clade easily distinguished from species of Akanthomyces sensu stricto, Beauveria and Cordyceps. Within the Samsoniella clade, the majority of Samsoniella species grouped together, while only two strains, named as S. lepidopterorum, formed a separate branch with a relatively far genetic distance. Furthermore, the seven spider- pathogenic strains (RCEF 0643, RCEF 1481, RCEF 2831, RCEF 2868, RCEF 2588, RCEF 2830, RCEF 2595) and four insect- pathogenic strains (RCEF2590, RCEF 2592, RCEF 2870, RCEF 5406) in this study are located on different branches of the Samsoniella clade. Strains RCEF 0643 and S. alpina were clustered in the same branch (MLBP=98, PP=1.00). Strain RCEF 2592 and RCEF 2595 were grouped with S. erucae clade (MLBP=95,PP=1.00). Strain RCEF 1481 was clustered in the same clade with S. hepiali (MLBP=100,PP=1.00). However, another seven strains formed three independent branches. S. fusiformispora (RCEF 5406 and RCEF 2588) formed a monophyletic group which closely clustered with S. hymenopterorum and S. farinosa with high bootstrap values. S. aranea (RCEF 2831 RCEF 2868, and RCEF 2870) clustered in an independent branch, which was phylogenetically close to S. yunnanensis (MLBP=100,PP=1.00). S. anhuiensis (RCEF 2830 and RCEF 2590) formed an independent sister branch with high support(MLBP=97, PP=0.97). Five-gene phylogenetic analyses suggested that RCEF 0643, RCEF 1481, RCEF 2592, and RCEF 2595 were known species. However, the other seven strains were three new species in Samsoniella.

Taxonomy

Samsoniella anhuiensis T. Wang, Ming J. Chen & B. Huang, sp. nov.

MycoBank No: 849801
Fig. 2

Etymology

Named after the location Anhui Province where the species was originally collected.

Typification

China. Anhui Province: Xuancheng City, the Jingting Mountains National Forest Park, on a spider attached to a leaf, 15 March 2006, Mingjun Chen & Xueqiu Zhao, holotype XC20060315-06. Sequences from strain RCEF2830 and RCEF2590 have been submitted to GenBank with accession numbers. RCEF2830: SSU = OM268844; LSU = OM268849; TEF = OM483865; RPB1 = OM751889. RCEF2590: SSU = OR978313; LSU = OR978316; TEF = OR966516; RPB1 = OR989964.

Description

Sexual morph : Undetermined. Asexual morph: Isaria-like. Synnemata arising from the whole body of spider, white, flexuous, multiple, fleshy, up to 12 mm long, with terminal branched, white conidia produced from the branches of synnemata, powdery and floccose (Fig. 2A). Conidiophores arising from the aerial and prostrate hyphae, solitary and verticillate. Phialides in whorls of 2–5, 5.0–15.2 × 1.5–2.3 μm, smooth-walled, with basal portion swollen to ellipsoidal, tapering into a distinct neck, 1.8–5.2 × 0.8–1.2 μm. Conidia in chains, spherical to elliptical, aseptate, hyaline, 2.1–3.2 × 1.3–2.2 μm.

Figure 2. 

Samsoniella anhuiensis A fungus on spider B colony on SDAY/4 C colony on PDA D, F conidiophores structure and conidia on SDAY/4 E, G conidiophores structure and conidia on PDA. Scale bars: 15 mm (B, C); 10 μm (D–G).

Culture characteristics

Colonies on 1/4 SDAY, attaining a diam 38–42 mm in 14 d at 25 °C. Colonies white, with smooth and neat edge, with high mycelial density at the centrum (Fig. 2B). Reverse pale yellow to yellowish, appears flesh pink at 30 d. Hyphae smooth, septate, hyaline, 1.5–2.3 μm width. Erect conidiophores usually arising from aerial hyphae, with phialides in whorls of two to three or occasionally with solitary phialides along the hyphae. Phialides basal portion cylindrical, tapering to a distinct neck, 4.8–16.0 μm long, 1.4–2.0 μm basal width and 0.6–1.0 μm distinct neck width. Conidia in (Fig. 2D), smooth-walled, hyaline, spherical to elliptical, ovoid, occasionally pointed at both ends, 2.4–3.2 × 1.5–2.1 μm (Fig. 2F). Chlamydospores and synnemata not observed.

Colonies on PDA, 39–41mm diameter in 14 d at 25 °C, white. The central part of the colony is raised and appears light yellowish (Fig. 2C). Reverse yellowish in the center. Hyphae smooth, septate, hyaline, with septum and branches, 1.5–2.8 μm width, with phialides in whorls of two to five. Phialides basal portion cylindrical, tapering to a distinct neck, (7-)8–11.5(-13) μm long, 1.3–2.2 μm basal width and 0.5–0.8 μm distinct neck width (Fig. 2E). Conidia in chains, 1-celled, smooth-walled, hyaline, fusiform, elliptical, to obovate, 2–3(-3.5) × 1–2.5 μm (Fig. 2G).

Habitat

Occurring on spider attached to the upperside of tree leaf.

Notes

Samsoniella anhuiensis was easily identified as belonging to Samsoniella based on the phylogenetic analyses (Fig. 1). Based on the combined multigene dataset, S. anhuiensis has an independent branch and has a close relationship with S. tiankengensis. However, colonies of S. tiankengensis exhibit a faster growth rate on PDA compared to S. anhuiensis, displaying white to light pink colonies with a light yellowish reverse. In contrast, colonies of S. anhuiensis appear light yellowish and take on a flesh-pink hue at 30 days on 1/4 SDAY, with a yellowish center in reverse. Notably, S. anhuiensis distinguishes itself from S. tiankengensis through the presence of larger spherical, elliptical to ovoid conidia (Table 2).

Table 2.
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Morphological comparison of three new species with other related Samsoniella species (Wang et al. 2022).

Species Morphological characteristics Reference
Synnemata (mm) Conidiophores (μm) Colony growth rate (mm)(14d, 25 °C) Phialide Phialides size (μm) Conidia (μm) Hosts/substrates
S. anhuiensis white, flexuous, multiple, fleshy, up to 12, with terminal branched - 39–41 verticillate, in whorls of 2 to 5 8.0–11.5 × 1.3–2.2, , wide (apex) 0.5–0.8, basal portion cylindrical to narrowly lageniform Fusiform, spherical, to obovate 2.0–3.5 × 1.0–2.5 spider this study
S. alpina irregularly branched, 3–20 long, cylindrical or clavate stipes with white powdery heads 3.1–6.5 × 1.6–2.8 up to 40 verticillate on conidiophores, solitary or verticillate on hyphae 4.7–9.5 × 1.9–3.1, wide (apex) 0.5–1.1, basal portion cylindrical to narrowly lageniform fusiform or oval 2.0–3.1 × 1.3–2.1 larvae of Hepialus baimaensis Wang et al. 2020a
S. aranea Synnemata not observed - 34.5–36 verticillate, in whorls of 2 to 4 6.9–11.2 × 1.4–1.9, wide (apex) 0.5–0.9, basal portion cylindrical to narrowly lageniform elliptical, fusiform 1.9–3.4 × 1.2–2.4 spider this study
S. coleopterorum Synnemata not observed - 36–40 verticillate, in whorls of 2 to 4 5.4–9.7 × 1.2–1.8, a cylindrical to ellipsoidal basal portion fusiform, ellipsoidal or subglobose 1.7–2.5 × 1.2–1.8 Snout beetle Curculionidae Chen et al. 2020
S. erucae branched or unbranched, fleshy - 46–48 solitary or in groups of three 6.8 -13.7 × 1.1 -1.5 with a cylindrical or ellipsoidal basal portion and tapered into a short, distinct neck fusiform to ellipsoidal 2.3–2.9 × 1.1–1.5 caterpillar Lepidoptera Chen et al. 2022
S. fusiformispora multiple, unbranched, 2–3 long - 36.5–39 verticillate, in whorls of 2 to 5 7.4–16.0 × 1.3–1.9, wide (apex) 0.5–1.0, basal portion cylindrical to narrowly lageniform fusiform 1.9–3.4 × 1.2–2.4 spider this study
S. hepiali branched or unbranched, 5–41long 4.0–7.6 × 1.4–2.2 50–55 verticillate, in whorls of 2 to 5, solitary or opposite on hyphae 3.5–13.6 × 1.3–2.1, wide (apex) 0.5–1.0, basal portion cylindrical to narrowly lageniform fusiform or oval 1.8–3.3 × 1.4–2.2 larvae of Hepialus armoricanus Wang et al. 2020a
S. tiankengensis branched or unbranched, fleshy - 53–56 solitary or in groups of four 5.4–10.4 × 1.3–2.2, cylindrical or subellipsoidal basal portion and tapered into a short, distinct neck ellipsoidal 2.3–2.8 × 1.6–1.8 pupa of Lepidoptera Chen et al. 2022
S. yunnanensis gregarious, flexuous, fleshy, 4.0–18.0 long, with terminal branches of 3–7 × 1.0–2.0 4.2–23.5 × 1.4–2.3 48–50 verticillate, in whorls of 2 to 7, usually solitary on hyphae 4.5–11.6 × 1.2–2.4, wide (apex) 0.6–1.0, basal portion cylindrical to narrowly lageniform fusiform or oval 2.0–3.3 × 1.1–2.2 pupa of Limacodidae Wang et al. 2020a

Samsoniella aranea T. Wang, Ming J. Chen & B. Huang, sp. nov.

MycoBank No: 849800
Fig. 3

Etymology

Referring to its host, spider, family Araneae.

Typification

China. Anhui Province: Xuancheng City, the Jingting Mountains National Forest Park, on spiders, in the litter layer, 15 March 2006 and 27 April 2006, Mingjun Chen & Xueqiu Zhao, holotype XC20060427-06, ex-holotype XC20060315-12. Sequences from strains RCEF2868, RCEF2831 and RCEF 2870 have been submitted to GenBank with accession numbers: RCEF2868: SSU = OM268846; LSU = OM268851; TEF = OM483867; RPB1 = OM751883; RPB2 = OM802501. RCEF2831: SSU = OM268845; LSU = OM268850; TEF = OM483866; RPB1 = OM751882; RPB2 = OM802500. RCEF 2870: SSU = OR978314; LSU = O978317; TEF = OR966517; RPB1 = OR989965; RPB2 = OR989966.

Description

Sexual morph : Undetermined. Asexual morph: Isaria-like. Mycellium on the spider consisting of white, smooth, branched, septate, 1.6–2.5 μm diam hyphae (Fig. 3A). Conidiophores solitary, arising from superficial hyphae, smooth, cylindrical, flexuous. Phialides verticillate, in whorl of 2–4, 5.0–12.6 × 1.2–2.3 μm, with basal portion swollen to ellipsoidal, tapering into a distinct neck, 4.0–6.0 × 0.8–1.0μm. Conidia in chains, fusiform, aseptate, hyaline, 2.1–3.6 × 1.5–2.4 μm.

Figure 3. 

Samsoniella aranea A fungus on spider B colony on SDAY/4 C colony on PDA D, G conidiophores structure and conidia on SDAY/4 E, F conidiophores structure and conidia on PDA. Scale bars: 15 mm (B, C); 10 μm (D–G).

Culture characteristics

Colonies on 1/4 SDAY, attaining a diam of 34.5–41.0 mm in 14 d at 25 °C, floccose, colonies white to cream-yellowish, with white smooth and neat edge (Fig. 3B), reverse light yellowish, sporulating abundantly. Hyphae smooth-walled, branched, hyaline, septate, 1.5–2.3 μm wide. Conidiophores smooth-walled, cylindrical, verticillate, 4.8–16.0 × 1.4–2.0 μm. Phialides in whorls of two to four, usually solitary on hyphae, basal portion cylindrical, tapering to a distinct neck; 5.1–16.9 μm long, 1.3–2.1 μm wide at the base, and 0.5–1.0 μm wide at the apex (Fig. 3D). Conidia in chains, smooth-walled, hyaline, elliptical, occasionally fusiform, 1.9–3.5 × 1.4–2.6 μm (Fig. 3G). Chlamydospores and synnemata not observed.

Colonies on PDA, attaining a diam of 34.5–36 mm in 14 d at 25 °C, floccose, colonies white to cream-yellowish, with a white smooth and neat edge, forming radial folds from the center outwards (Fig. 3C). Reverse yolk yellowish, sporulating abundantly. Hyphae smooth walled, branched, hyaline, septate, 1.5–2.6 μm wide. Conidiophores smooth – walled, cylindrical, verticillate. Phialides in whorls of two to four, usually solitary on hyphae, basal portion cylindrical, tapering to a distinct neck; 6.9–11.2 μm long, 1.4–1.9 μm wide at the base, and 0.5–0.9μm wide at the apex (Fig. 3E). Conidia 1-celled, in chains, smooth-walled, hyaline, elliptical, occasionally fusiform, 1.9–3.4 × 1.2–2.4 μm (Fig. 3F).

Habitat

Occurring on spiders in the litter layer.

Notes

Samsoniella aranea was readily classified within the genus Samsoniella through phylogenetic analyses (Fig. 1). Analysis of the combined multigene dataset unveiled that S. aranea forms an independent branch and shares a close relationship with S. yunnanensis. However, notable distinctions were observed between the two species. Unlike S. yunnanensis, where synnemata arise from insect cocoons, synnemata of S. aranea were not observed. Additionally, distinct growth characteristics were noted, with colonies of S. yunnanensis exhibiting a faster growth rate on PDA compared to S. aranea. Morphological differences were evident in the colonies on PDA, with S. aranea colonies being floccose, white to cream-yellowish, and having a yolk-yellowish reverse. On the other hand, colonies of S. yunnanensis were described as loose and hairy, appearing white with a reddish-brown reverse.

Samsoniella fusiformispora T. Wang, Ming J. Chen & B. Huang, sp. nov.

MycoBank No: 849799
Fig. 4

Etymology

Referring to the typical fusiform conidia.

Typification

China. Gansu Province: Tianshui City, Maiji National Forest Park, on a spider, underside of tree leaf, 22 September 2010, Wang Liming, holotype MJS20100922-21. Sequences from strain RCEF5406 and RCEF2588 submitted to GenBank with accession numbers. RCEF5406: SSU = OM268843; LSU = OM268848; TEF = OM483864; RPB1 = OM751890. RCEF2588: SSU = OR978312; LSU = OR978315; TEF = OR966515.

Description

Sexual morph : Undetermined. Asexual morph: Isaria-like. Synnemata multiple, unbranched, arising from the whole body of spider, 3–6 mm long, Stipes cylindrical or clavate, 0.5–1.0 mm wide, pale yellowish, white conidia produced from the synnemaya and hyphal layer (Fig. 4A). Phialides verticillate, in whorl of 2–5, 5.0–12.0 × 1.9–2.8 μm, with basal portion swollen to ellipsoidal, tapering into a distinct neck, 2.3 -3.8 × 0.5–1.2 μm. Conidia in chains, fusiform, aseptate, hyaline, 2.1–3.5 × 1.6–2.2 μm.

Figure 4. 

Samsoniella fusiformispora A fungus on spider B colony on SDAY/4 C colony on PDA D, F conidiophores structure and conidia on SDAY/4 E, G conidiophores structure and conidia on PDA. Scale bars: 15 mm (B, C); 10 μm (D–G).

Culture characteristics

Colonies on 1/4 SDAY fast-growing, 39.5–44 mm diameter in 14 d at 25 °C, colonies white edge to yellowish center, cottony (Fig. 4B), reverse yellow to orange-yellow, hyphae smooth – walled, branched, hyaline, septate, 1.7–2.6 μm wide. Conidiophores smooth-walled, cylindrical, verticillate. Phialides in whorls of three to five, usually solitary on hyphae, basal portion cylindrical, tapering to a distinct neck; 7.6–15 μm long, 1.9–2.6 μm wide at the base, and 0.7–1.2 μm wide at the apex (Fig. 4D). Conidia in chains, smooth-walled, hyaline, fusiform, 2.1–3.6(-4.4) × 1.8–2.2 μm (Fig. 4F). Chlamydospores and synnemata not observed. Size and shape of phialides and conidia similar in culture. Sexual state not observed.

Colonies on PDA, attaining a diam of 36.5–39 mm in 14 d at 25 °C, floccose, colonies white to yellowish, with high mycelial density at the centrum (Fig. 4C). Reverse pale yellowish edge to orang center. Hyphae smooth- walled, branched, hyaline, septate, 1.5–2.5 μm wide. Conidiophores smooth – walled, cylindrical, verticillate. Phialides in whorls of two to five, usually solitary on hyphae, basal portion cylindrical, tapering to a distinct neck; 7.4–16(–26) μm long, 1.3–1.9(–2.4) μm wide at the base, and 0.5–1.0 μm wide at the apex (Fig. 4E). Conidia 1-celled, in chains, smooth-walled, hyaline, fusiform, 1.9–3.4 × 1.2–2.4 μm (Fig. 4G).

Habitat

Occurring on spider attached to the underside of tree leaf.

Notes

Samsoniella fusiformispora was unequivocally identified as a member of the Samsoniella genus through phylogenetic analyses (Fig. 1) and was found to share a close relationship with S. coleopterorum. However, upon further investigation and comparison of the morphological characteristics of the three new species with other related Samsoniella species (Table 2), distinct differences emerged. Colonies of S. fusiformispora were noted to be white to yellowish, with a pale yellowish edge transitioning to an orange center in reverse. In contrast, colonies of S. coleopterorum were observed to be white, with a yellowish reverse.

Discussion

The typical characteristics of Samsoniella were oval to fusiform conidia, bright red-orange stromata of the sexual morphs and synnemata of the asexual morphs (Chen et al. 2020). In this study, we present a phylogenetic investigation of cordycipitaceous Isaria-like fungi pathogenic on spiders. Combined with microscopic characteristics and phylogenetic analysis based on multi-locus sequence data, S. fusiformispora, S. aranea and S. anhuiensis were described and illustrated as new species in Samsoniella. It was found that the hosts of most reported Samsoniella species are Lepidoptera larvae or pupae, while the host of S. coleopterorum is a snout beetle (Curculionidae), and the host of S. hymenopterorum is a bee (Mongkolsamrit et al. 2018; Chen et al. 2020; Wang et al. 2020a). However, it should be noted that Wang et al. (2020a) described the host of S. hymenopterorum as being “Bee, family Vespidae”. The family Vespidae are wasps, not bees. Our study has expanded the hosts of Samsoniella from Insecta to Arachnida.

Generally, the phialides of S. fusiformispora were longer and thinner than those of the closely-related S. coleopterorum while they also had bigger typical fusiform conidia with greater length to width ratio. In the ML and BI phylogenetic trees, S. aranea was inferred as a phylogenetic sister of S. yunnanensis with strong support (93%/1.00) and distinct from other related species in Samsoniella. The synnemata of S. aranea was not observed, but S. yunnanensis has gregarious, flexuous and fleshy synnemata arising from the limacodid cocoons (Wang et al. 2020a). Furthermore S. yunnanensis has smaller fusiform to oval conidia than S. aranea and the colonies on PDA grow faster than S. aranea. Similarly, S. anhuiensis was easily separated by the phylogenetic analyses with independent branches in the phylogenetic tree.

Kepler et al. (2017) found that sequences of Isaria sp. spat 09-050 and Isaria sp. spat 09-051 were firstly obtained, and two strains were clustered as the phylogenetic sister of Isaria spp. with 100 bootstrap proportion in the weighted parsimony (WP) analytic tree based on five genes (SSU, LSU, TEF, RPB1 and RPB2), which was classified as Akanthomyces group. Then Wang et al. (2020a) constructed the multigene phylogenetic tree studied the new taxa of the family Cordycipitaceae and the new systematic position of the Chinese cordycipitoid fungus Paecilomyces hepiali. In this multigene phylogenetic tree, Isaria sp. spat 09-050 and Isaria sp. spat 09-051 were clustered in genus Samsoniella as sister group of S. vallis but in two independent branches. In this study, we obtained the same results. We convinced that Isaria sp. spat 09-050 and Isaria sp. spat 09-051 is an unpublished new species of the Samsoniella, should be revised to Samsoniella sp. spat 09-050 and Samsoniella sp. spat 09-051.

In this study, based on morphological characteristics and five loci phylogenetic analysis, S. anhuiensis, S. aranea and S. fusiformispora were separated from other Samsoniella species, which are described here as new species. The strain RCEF0643 was identified as S. alpina, the strain RCEF1481 was named as S. hepiali, and the strains RCEF2592 and RCEF 2590 was identified as S. erucae. Furthermore, our study significantly broadens the host range of Samsoniella from Insecta to Arachnida, marking a noteworthy expansion in understanding the ecological associations of these fungi. Additionally, the identification of both mononematous and synnematous conidiophores in our study not only expands the knowledge of Samsoniella species but also provides a basis for future research by comparing the ecological significance between these conidiophore types.

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 National Natural Science Foundation of China (Nos. 32172473 and 31972332).

Author contributions

MC and BH conceived and designed the study. TW and MC wrote the manuscript, conducted the experiments, and analyzed the data. JL, and XC did a part of the experiments. Zl and NH edited the manuscript. MC and BH edited the manuscript and supervised the project.

Author ORCIDs

Ting Wang https://orcid.org/0000-0002-9296-7280

Jun Li https://orcid.org/0009-0009-3183-2604

Xiaoyun Chang https://orcid.org/0000-0002-0093-9582

Zengzhi Li https://orcid.org/0000-0002-9606-5030

Nigel L. Hywel-Jones https://orcid.org/0009-0004-8219-3682

Bo Huang https://orcid.org/0000-0001-6032-7396

Mingjun Chen https://orcid.org/0000-0002-1439-7796

Data availability

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

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