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Research Article
Acremonium capsici and A. guizhouense, two new members of Acremonium (Hypocreales, Sordariomycetes) isolated from the rhizosphere soil of Capsicum annuum
expand article infoShuo-Qiu Tong‡, Lei Peng‡, Yong-Jun Wu‡
‡ Guizhou University, Guiyang, China

Corresponding author: Yong-Jun Wu ( wyjbio@163.com )

Academic editor: Huzefa Raja
© 2023 Shuo-Qiu Tong, Lei Peng, Yong-Jun Wu.
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: Tong S-Q, Peng L, Wu Y-J (2023) Acremonium capsici and A. guizhouense, two new members of Acremonium (Hypocreales, Sordariomycetes) isolated from the rhizosphere soil of Capsicum annuum. MycoKeys 95: 1-13. https://doi.org/10.3897/mycokeys.95.97062
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Abstract

Two new species, Acremonium capsici and A. guizhouense, isolated from the rhizosphere soil of Capsicum annuum, are described and illustrated. Two-locus DNA sequences based on phylogeny, in combination with the morphology of the asexual morph, were used to characterize these species. In the phylogenetic tree, both new species clustered into a monophyletic clade with strong support, distinct from other previously known species of Acremonium. The new species differed from their allied species in their morphology.

Keywords

filamentous fungi, morphology, new species, phylogeny, taxonomy

Introduction

Capsicum annuum L. is a globally grown and consumed spice crop that is rich in vitamins. C. annuum originated from the tropical and subtropical regions of Central and South America. It was introduced into China at the end of the Ming Dynasty, and has a long history of cultivation in China. According to the Food and Agriculture Organization of the United Nations, global C. annuum production reached approximately 36.1 million ton in 2020, with China producing the most in the world.

Link (1809) erected the genus Acremonium, whose members are geographically widespread and involve many substrates (Yang et al. 2019). As described by Gams (1971), the main diagnostic criteria of the genus Acremonium are conidiophores simple or verticillate; phialides narrow, solitary, generally cylindrical and gradually tapered towards the tips; conidia unicellular, hyaline to light-pigmented, spherical to cylindrical, arranged in slimy heads or unconnected chains or both; chlamydospores and sclerotia present or absent. The genus Acremonium is similar to some genera – Sarocladium W. Gams & D. Hawksw., Brunneomyces Giraldo, Gené & Guarro, and Chordomyces Bilanenko, M.L. Georgieva & Grum-Grzhimaylo etc. (Giraldo et al. 2015, 2017), including some of the simplest morphologies of all filamentous anamorphic fungi (Summerbell et al. 2011), so the morphological delimitation between them is challenging (Yang et al. 2019). Recent phylogenetic studies have documented that the genus Acremonium is polyphyletic, including sexual and nomenclaturally complex asexual morphs (Summerbell et al. 2011; Giraldo et al. 2012). To date, Acremonium has 219 records in the Index Fungorum (http://www.indexfungorum.org/Names/Names.asp, retrieval on Dec. 2022). However, many Acremonium taxa have been reported, but there are no trustworthy classification systems and little sequence data are available in GenBank for multigene analyses (Park et al. 2017). In the future, the classification of Acremonium will become clearer with the increase of molecular data.

In this study, seven strains of Acremonium were isolated in the process of investigating the rhizosphere fungal diversity of cultivated Capsicum annuum in Guizhou Province, southwest China, based on a culturable method. Identification of these strains in combination with morphological characteristics and phylogenetic analysis showed that these strains belong to two previously undescribed species of Acremonium. The new species differed from their allied species in their morphology.

Materials and methods

Fungal isolation and morphology

Capsicum annuum plants were cultivated in farmlands located in Guiyang, Guizhou Province, China (26°45'75"N, 106°64'87"E). One composite rhizosphere soil sample was taken from five randomly selected C. annuum plants. The roots were shaken vigorously to separate soil that is not tightly attached to the roots, and the remaining soil attached to the region 2–3 mm from the plant root was collected as the rhizosphere soil sample (Smalla et al. 2001). Fungi were isolated and purified using a dilution plate method as follows: 2 g samples were weighed with glass beads in a conical flask containing 20 mL sterile water, mixed evenly using eddy shock for 10 min, diluted to 1:10,000, and cultured on Martin’s medium supplemented with chloramphenicol and cycloheximide.

The purified isolates were transferred to potato dextrose agar (PDA), oatmeal agar (OA), malt extract agar (MEA), and corn meal agar (CMA) at 25 °C in darkness for 14 days to examine the macroscopic and morphological characteristics of the colonies. Photomicrographs of the diagnostic structures were obtained using an OLYMPUS BX53 microscope equipped with differential interference contrast optics, an OLYMPUS DP73 high-definition color camera, and cellSens software v.1.18. Both dry and living cultures were deposited at the Institute of Agro-bioengineering, Guizhou University.

DNA extraction, PCR amplification, and sequencing

Total DNA was extracted from each of the new isolates using the BioTeke Fungus Genomic DNA Extraction kit (DP2032, BioTeke, Beijing, China) according to the manufacturer’s instructions. According to Li et al. (2022), the internal transcribed spacers (ITS), the 28S nrRNA locus (LSU), translation elongation factor 1-alpha gene region (TEF 1-α), RNA polymerase II second largest subunit gene (RPB2), and small subunit rDNA (SSU) were amplified and sequenced using ITS1/ITS4 (White et al. 1990), LROR/LR7 (Vilgalys and Hester 1990), EF1-983F/EF1-2218R (Rehner and Buckley 2005), fRPB2-5f/fRPB2-7cR (Liu et al. 1999), and NS1/NS4 (White et al. 1990) primers, respectively. All new sequences were submitted to GenBank (Table 1).

Table 1.
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Strains included in the present study.

Species Strains LSU ITS SSU TEF 1-α RPB2
Acremonium alternatum CBS 407.66 T HQ231988 HE798150
Acremonium alternatum CBS 831.97 HQ231989
Acremonium arthrinii MFLU 18-1225 T MN036334 MN036335 MN038169
Acremonium behniae CBS 146824 T MW175400 MW175360
Acremonium biseptum CBS 750.69 T HQ231998
Acremonium blochii CBS 993.69 HQ232002 HE608636
Acremonium borodinense CBS 101148 T HQ232003 HE608635
Acremonium brachypenium CBS 866.73 T HQ232004 AB540570
Acremonium camptosporum CBS 756.69 T HQ232008 HQ232186
Acremonium cavaraeanum CBS 101149 T HF680202 HF680220
Acremonium cavaraeanum CBS 111656 HF680203 HF680221
Acremonium cavaraeanum CBS 758.69 HQ232012 HF680222
Acremonium cerealis CBS 207.65 HQ232013
Acremonium cerealis CBS 215.69 HQ232014
Acremonium chiangraiense MFLUCC 14-0397 T MN648329 MN648324
Acremonium chrysogenum CBS 144.62 T HQ232017 HQ232187
Acremonium chrysogenum CBS 401.65 MH870276 MH858636
Acremonium citrinum CBS 384.96 T HF680217 HF680236
Acremonium curvum CGMCC 3.20954 T ON041050 ON041034 ON876754 ON494579 ON494583
Acremonium dimorphosporum CBS 139050 T LN810506 LN810515
Acremonium exiguum CBS 587.73 T HQ232035
Acremonium exuviarum UAMH 9995 T HQ232036 AY882946
Acremonium felinum CBS 147.81 T AB540488 AB540562
Acremonium flavum CBS 596.70 T HQ232037 HQ232191
Acremonium flavum CBS 316.72 MH872204 MH860487
Acremonium fuci CBS 112868 T AY632653
Acremonium fuci CBS 113889 AY632652
Acremonium fusidioides CBS 109069 HF680204 HF680223
Acremonium fusidioides CBS 991.69 HF680211 HF680230
Acremonium fusidioides CBS 840.68 T HQ232039 FN706542
Acremonium globosisporum CGMCC 3.20955 T ON041051 ON041035 ON876755 ON494580 ON494584
Acremonium globosisporum GZUIFR 22.037 ON041052 ON041036 ON876756 ON494581 ON494585
Acremonium globosisporum GZUIFR 22.038 ON041053 ON041037 ON876757 ON494582 ON494586
Acremonium hansfordii CBS 390.73 HQ232043 AB540578
Acremonium hennebertii CBS 768.69 T HQ232044 HF680238
Acremonium inflatum CBS 212.69 T HQ232050
Acremonium mali ACCC 39305 T MF993114 MF987658
Acremonium moniliforme CBS 139051 T LN810507 LN810516
Acremonium moniliforme FMR 10363 LN810508 LN810517
Acremonium parvum CBS 381.70A HQ231986 HF680219
Acremonium persicinum CBS 310.59 T HQ232077
Acremonium persicinum CBS 101694 HQ232085
Acremonium pinkertoniae CBS 157.70 T HQ232089 HQ232202
Acremonium polychroma CBS 181.27 T HQ232091 AB540567
Acremonium potronii CBS 189.70 HQ232094
Acremonium pseudozeylanicum CBS 560.73 T HQ232101
Acremonium pteridii CBS 782.69 T HQ232102
Acremonium pteridii CBS 784.69 HQ232103
Acremonium sclerotigenum CBS 124.42 T HQ232126 FN706552 HQ232209
Acremonium sclerotigenum A101 KC987215 KC987139 KC987177 KC998961
Acremonium sclerotigenum A130 KC987242 KC987166 KC987204 KC998988
Acremonium sp. E102 KC987248 KC987172 KC987210 KC998994 KC999030
Acremonium spinosum CBS 136.33 T HQ232137 HE608637 HQ232210
Acremonium stroudii CBS 138820 T KM225291
Acremonium tumulicola CBS 127532 T AB540478 AB540552
Acremonium variecolor CBS 130360 T HE608651 HE608647
Acremonium variecolor CBS 130361 HE608652 HE608648
Acremonium verruculosum CBS 989.69 T HQ232150
Acremonium capsici SQT01 T OP740978 OP703286 OP750190 OP757287 OP730522
Acremonium capsici SQT02 OP740979 OP703287 OP750191 OP757288 OP730523
Acremonium capsici SQT03 OP740980 OP703288 OP750192 OP757289 OP730524
Acremonium guizhouense SQT04 T OP740981 OP703289 OP750193 OP757290 OP730525
Acremonium guizhouense SQT05 OP740982 OP703290 OP750194 OP757291 OP730526
Acremonium guizhouense SQT06 OP740983 OP703291 OP750195 OP757292 OP730527
Acremonium guizhouense SQT07 OP740984 OP703292 OP750196 OP757293 OP730528
Bryocentria brongniartii M139 EU940105 EU940052
Bryocentria brongniartii M190 EU940125 EU940052
Bryocentria metzgeriae M140 EU940106
Bulbithecium hyalosporum CBS 318.91 T AF096187 HE608634
Cephalosporium purpurascens CBS 149.62 T HQ232071
Cosmospora lavitskiae CBS 530.68 T HQ231997
Emericellopsis alkalina CBS 127350 T KC987247 KC987171 KC987209 KC998993 KC999029
Emericellopsis terricola CBS 120.40 T U57082 U57676 U44112
Gliomastix roseogrisea CBS 134.56 T HQ232121
Hapsidospora irregularis ATCC 22087 T AF096192 AF096177
Kiflimonium curvulum CBS 430.66 T HQ232026 HE608638 HQ232188
Lanatonectria flavolanata CBS 230.31 HQ232157
Leucosphaerina arxii CBS 737.84 T HE608662 HE608640
Nigrosabulum globosum ATCC 22102 T AF096195
Paracremonium contagium CBS 110348 T HQ232118 KM231831 KM231966
Parasarocladium breve CBS 150.62 T HQ232005
Parasarocladium radiatum CBS 142.62 T HQ232104 HQ232205
Pestalotiopsis hawaiiensis CBS 114491 T KM116239 KM199339 KM199514
Pestalotiopsis spathulata CBS 356.86 T KM116236 KM199338 KM199513
Pseudoacremonium sacchari CBS 137990 T KJ869201 KJ869144
Sarcopodium vanillae CBS 100582 HQ232174 KM231780 KM231911
Sarocladium bacillisporum CBS 425.67 T HQ231992 HE608639 HQ232179
Sarocladium bactrocephalum CBS 749.69 T HQ231994 HG965006 HQ232180
Sarocladium strictum CBS 346.70 T HQ232141 AY214439 HQ232211
Sarocladium terricola CBS 243.59 T HQ232046 HQ232196
Selinia pulchra AR 2812 GQ505992 HM484859 HM484841
Trichothecium crotocinigenum CBS 129.64 T HQ232018 AJ621773
Trichothecium indicum CBS 123.78T AF096194 AF096179
Trichothecium roseum DAOM 208997 U69891 U69892
Trichothecium sympodiale ATCC 36477 U69889 U69890

Notes: “T” stands for Ex-type strains. New isolates are in bold and blue.

Phylogenetic analyses

In this study, we utilized sequence data mainly from recent publications (Yang et al. 2019; Li et al. 2022) and the sequenced new isolates (Table 1). According to Li et al. (2022) and Yang et al. (2019), Pestalotiopsis spathulata (CBS 356.86) and P. hawaiiensis (CBS 114491) were chosen as the outgroup taxa. The sequences were aligned using MAFFT v7.037 (Katoh and Standley 2013) and adjusted using MEGA 6.06 (Tamura et al. 2013). The aligned sequences of LSU and ITS were concatenated using PhyloSuite v1.16 (Zhang et al. 2020).

The best-fit substitution model was selected using the corrected Akaike information criterion, in ModelFinder (Kalyaanamoorthy et al. 2017). The maximum likelihood (ML) and Bayesian inference (BI) methods were used in the analysis. The ML analysis was implemented in IQ-TREE v1.6.11 (Nguyen et al. 2015) with 10,000 bootstrap tests, using the ultrafast algorithm (Minh et al. 2013). For the BI, MrBayes v3.2 (Ronquist et al. 2012) was used and Markov chain Monte Carlo simulations were run for 5,000,000 generations with a sampling frequency of every 500 generations and a burn-in of 25%. The above analyses were carried out in PhyloSuite v1.16 (Zhang et al. 2020).

Results

Phylogenetic analyses

Ninety-five isolates (including the seven with new sequence data) were included in our dataset (Table 1), which comprised 976 positions (including gaps), of which 377 were phylogenetically informative (122 of LSU and 255 of ITS). For Maximum-likelihood analyses, IQ-TREE’s ModelFinder under the corrected Akaike information criterion (AICc) proposed a TN+F+I+G4 for LSU, GTR+F+I+G4 for ITS. For Bayesian analysis, IQ-TREE’s ModelFinder under the AICc proposed a GTR+F+G4 for LSU, GTR+F+I+G4 for ITS. The results show that the isolates SQT01, SQT02, and SQT03 clustered in a single clade with high support (ML BS 100/BI pp 1), and were closely related to Acremonium variecolor (Fig. 1). The isolates SQT04, SQT05, SQT06, and SQT07 also clustered in a single clade with high support (100/0.98), and were closely related to A. persicinum and A. verruculosum (Fig. 1).

Figure 1. 

Phylogram generated from maximum likelihood analysis based on LSU + ITS sequence data. Bootstrap support values of maximum likelihood higher than 75% and Bayesian posterior probabilities greater than 0.75 are given above each branch. The new collection is highlighted in blue bold. Clades are identified using clade nomenclature formally defined by Summerbell et al. (2011), and Yang et al. (2019). Ex-type strains are indicated by “T”.

Taxonomy

Acremonium capsici S.Q. Tong & Y.J. Wu, sp. nov.

MycoBank No: 846330
Fig. 2

Etymology

Referring to the type strain isolated from the rhizosphere soil of Capsicum annuum.

Type

Guiyang City, Guizhou Province, China 26°45'75"N, 106°64'87"E, isolated from the rhizosphere soil of Capsicum annuum, August 2022, Shuo-Qiu Tong (dried holotype culture SQT H-01, ex-holotype culture SQT01). GenBank: ITS = OP703286; LSU = OP740978; SSU = OP750190; TEF 1-α = OP757287; RPB2 = OP730522.

Description

Culture characteristics (14 days at 25 °C) – Colonies on PDA 20–21 mm diam, white, hairy, flat, radially striated, with a regular edge; reverse white. Colonies on MEA 18–19 mm in diameter, white, floccose, radially striated, with a regular edge; reverse white. Colonies on OA 18–19 mm in diameter, pale white, flat, with regular edge; reverse pale white. Colonies on CMA 18–19 mm in diameter, pale white, felty, with regular edge; reverse pale white. Hyphae hyaline, smooth, septate, branched, 1.0–2.5 µm wide. Phialides straight to flexuous, hyaline, smooth, arising from superficial hyphae, from hyphal strands or from hyphal coils, 20–42 μm (n = 50) long, 1–2 μm (n = 50) wide at the base. Conidia arranged in slimy heads, one-celled, ovoid to ellipsoidal, fusiform, 2.0–3.5 × 1.5–2.0 µm (n = 50), hyaline, smooth, or rough. Chlamydospores and teleomorph were not observed.

Additional specimens examined

Guiyang City, Guizhou Province, China 26°45'75"N, 106°64'87"E, isolated from the rhizosphere soil of Capsicum annuum, August 2022, Shuo-Qiu Tong, SQT02, ibid., SQT03. GenBank: ITS = OP703287–OP703288; LSU = OP740979–OP740980; SSU = OP750191–OP750192; TEF 1-α = OP757288–OP757289; RPB2 = OP730523–OP730524.

Known distribution

Guiyang City, Guizhou Province, China.

Notes

In a phylogenetic tree based on LSU + ITS sequences, Acremonium capsici forms a separate clade sister to A. variecolor in Acremonium sensu lato (Bionectriaceae). In a comparison of LSU and ITS nucleotides, A. capsici (Type strain SQT01) has 93% and 83% similarity, in LSU (459/492 bp, one gap) and ITS (388/468 bp, 16 gaps), which is different from A. variecolor (CBS 130360). They are distinguished by the appearance of colonies on OA, MEA, and PDA: colonies of A. capsici grow slowly (less than 25 mm), and are white, while colonies of A. variecolor grow faster (more than 40 mm), and are white to yellowish (Giraldo et al. 2012). In addition, A. capsici bear simple phialides, while conidiophores of A. variecolor are mostly branched, bearing whorls of two to five phialides (Giraldo et al. 2012). A. variecolor produces sessile conidia, which is not seen in A. capsici (Giraldo et al. 2012).

Figure 2. 

Morphology of Acremonium capsici sp. nov. a–d colony on PDA, MEA, OA, and CMA after 14 days at 25 °C (upper surface and lower surface) e phialides f conidia g phialides arising from ropes of hyphae h phialides arising from hyphal coils. Scale bars: 10 μm (e–h).

Acremonium guizhouense S.Q. Tong & Y.J. Wu, sp. nov.

MycoBank No: 846331
Fig. 3

Etymology

Referring to the country where this fungus was first isolated.

Type

Guiyang City, Guizhou Province, China 26°45'75"N, 106°64'87"E, isolated from the rhizosphere soil of Capsicum annuum, August 2022, Shuo-Qiu Tong (dried holotype culture SQT H04, ex-holotype culture SQT04). GenBank: ITS = OP703289; LSU = OP740981; SSU = OP750193; TEF 1-α = OP757290; RPB2 = OP730525.

Description

Culture characteristics (14 days at 25 °C) – Colonies on PDA 16–19 mm in diameter, yellowish white to grayish yellow, flat, zonate, with regular edge; reverse brownish orange. Colonies on MEA 9–13 mm in diameter, yellowish white to white, compact, convex with papillate surface, margin dentate, aerial mycelia extremely sparse; reverse yellowish white to umber. Colonies on OA 14–16 mm in diameter, pale, felty, with regular edge; reverse pale white. Colonies on CMA 16–14 mm in diameter, pale white, felty, with regular edge; reverse pale white. Hyphae hyaline, smooth, septate, branched, 1.0–3.0 µm wide. Phialides straight to flexuous, hyaline, smooth, arising from hyphae, 15.5–33.5 μm (n = 50) long, 1.5–2.5 μm (n = 50) wide at the base. Conidia gathered in slimy heads, one-celled, ovoid to ellipsoidal, 2.5–3.0 × 3.5–5.0 µm (n = 50), hyaline, smooth or rough. Chlamydospores and teleomorph not observed.

Additional specimens examined

Guiyang City, Guizhou Province, China 26°45'75"N, 106°64'87"E, isolated from the rhizosphere soil of Capsicum annuum, August 2022, Shuo-Qiu Tong, SQT05 = SQT06, ibid., SQT07. GenBank: ITS = OP703290–OP703292; LSU = OP740982–OP740984; SSU = OP750194–OP750196; TEF 1-α = OP757291–OP757293; RPB2 = OP730526–OP730528.

Known distribution

Guiyang City, Guizhou Province, China.

Notes

Phylogenetic and morphological data (Figs 1, 3) support our isolates SQT04–SQT07 as new species of Acremonium. A. guizhouense is phylogenetically closely related to A. verruculosum and A. persicinum. However, they can be distinguished by their sequence similarity (97% similarity, 10 base pairs (bp) differences and two gaps in 497 bp of LSU in A. verruculosum CBS 989.69; 98% similarity, 12 base pairs (bp) differences, and four gaps in 809 bp of LSU in A. persicinum CBS310.59). Since A. verruculosum and A. persicinum lack ITS sequences, it was not possible to compare A. guizhouense with them. Morphologically, the conidia of A. verruculosum are long ellipsoidal to cylindrical, rather than ovoid to ellipsoidal in A. guizhouense (Gams 1971). A. verruculosum, on the other hand, has larger conidia than A. guizhouense (5.6–6.0 × 2.3–2.5 µm vs. 2.5–3.0 × 3.5–5.0 µm) (Gams 1971). Furthermore, conidia of A. verruculosum are catenulate, fusiform, pyriform to ellipsoidal rather than arranged as slimy heads, ovoid to ellipsoidal in A. guizhouense (Gams 1971). The conidia of A. guizhouense, on the other hand, are smaller than that of A. persicinum (2.5–3.0 × 3.5–5.0 µm vs. 3.2–4.8 × 1.2–3.0 µm) (Gams 1971).

Figure 3. 

Morphology of Acremonium guizhouense sp. nov. a–d colony on PDA, MEA, OA, and CMA after 14 days at 25 °C (upper surface and lower surface) e, f phialides and conidia g, h conidia are held together in slimy heads. Scale bars: 10 μm (e–h).

Discussion

Traditionally, a polyphasic approach based on morphology, physiology, biochemistry, or reactions to chemical tests, has been used to differentiate species (Senanayake et al. 2020). Currently, many new fungal taxa have been reported based on DNA sequences. Phylogenetic analysis is becoming increasingly important in reporting new taxa of fungi, and has gradually become a mandatory component. However, many previously published fungal taxa lack DNA molecular data, and even specimens have been lost (Zhang et al. 2022). Thus, there are still many undetermined, questionable, or misidentified taxa that warrant taxonomic investigations (Summerbell et al. 2018). Since most species of the genus Acremonium have only LSU and ITS sequences Li et al. (2022), we used only ribosomal sequences (LSU + ITS) for phylogenetic analysis, while the sequencing of other loci was aimed at establishing a database for future studies.

Members of the genus Acremonium are geographically widespread and ecologically diverse, and seem to colonize all types of substrates, including endophytes, epiphytes, saprophytes, human and plant pathogens, lichens, insects, or arthropods taxa (Yang et al. 2019). In addition, Acremonium species have various functions, such as biological control (Shang et al. 2018), enhancing drought tolerance of grasses, and promoting nectar production of beans (Jaber and Vidal 2009), as well as improving plant resistance to plant pathogens (Kasselaki et al. 2006). In the present study, all the isolates were obtained from the rhizosphere soils of Capsicum annuum. Therefore, more studies are necessary to further confirm their relationship with their host plant Capsicum annuum.

In summary, seven isolates of Acremonium were obtained from the rhizosphere soils of Capsicum annuum. Morphological characteristics in combination with two-locus (LSU + ITS) phylogenetic analysis were used for delimitation. Therefore, two new species of Acremonium capsici (three isolates) and Acremonium guizhouense (four isolates) are introduced. This study contributes to our understanding of the rhizosphere microbial population of Capsicum annuum and also of Acremonium species.

Acknowledgements

This study was financially supported by Guizhou Provincial Science and Technology Projects (Qian Ke He Zhi Cheng-ZK[2022] General 172, and ZK[2021] General 262), and Guizhou Provincial Institutions of higher learning Engineering Center Projects (Qian Jiao He KY[2021]006). We appreciate Charlesworth for English-language editing of the whole manuscript.

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