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Research Article
Multigene phylogeny, taxonomy, and potential biological properties of Pseudoroussoella and Neoroussoella species (Roussoellaceae, Dothideomycetes) from Asteraceae weeds in northern Thailand
expand article infoZin Hnin Htet‡, Kevin D. Hyde‡§|, Fatimah O. Alotibi|, Thilini K. W. Chethana‡, Ausana Mapook‡
‡ Mae Fah Luang University, Chiang Rai, Thailand
§ Zhongkai University of Agriculture and Engineering, Guangzhou, China
| King Saud University, Riyadh, Saudi Arabia

Corresponding author: Thilini K. W. Chethana ( kandawatte.thi@mfu.ac.th )

Corresponding author: Ausana Mapook ( phung.ausana@gmail.com )

Academic editor: Danushka Sandaruwan Tennakoon
© 2024 Zin Hnin Htet, Kevin D. Hyde, Fatimah O. Alotibi, Thilini K. W. Chethana, Ausana Mapook.
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: Htet ZH, Hyde KD, Alotibi FO, Chethana TKW, Mapook A (2024) Multigene phylogeny, taxonomy, and potential biological properties of Pseudoroussoella and Neoroussoella species (Roussoellaceae, Dothideomycetes) from Asteraceae weeds in northern Thailand. MycoKeys 111: 129-146. https://doi.org/10.3897/mycokeys.111.136922
Open Access

Abstract

In our study, dead stems of two Asteraceae species (weeds) were collected from northern Thailand. Both morphology and multigene phylogeny were used to determine the identity of the taxa. Maximum likelihood and Bayesian inference analyses of combined LSU, SSU, ITS, tef1-α and rpb2 data revealed two new species Pseudoroussoella bidenticola, and Neoroussoella chromolaenae with one new host record of N. entadae. Preliminary investigation into antibacterial properties revealed that our three isolates inhibited the growth of Bacillus subtilis, Escherichia coli, and Staphylococcus aureus. Additionally, we present updated phylogenetic trees for Roussoellaceae, accompanied by detailed descriptions and illustrations of the three identified species.

Key words

2 new species, antibacterial properties, Ascomycota, Bidens pilosa, Chromolaena odorata, new host record

Introduction

Asteraceae species exhibit a widespread distribution from polar to tropical regions (Xu et al. 2017). Many of these species hold economic significance, while others are categorized as weeds (Jansen and Palmer 1987; Katinas et al. 2007; Karlsson et al. 2008). In Thailand, numerous invasive weeds have an extensive spread, with Bidens pilosa and Chromolaena odorata being prevalent at roadsides, disturbed areas, and agricultural lands (Zungsontiporn et al. 2020). Mapook et al. (2020) studied the fungal diversity in Chromolaena odorata and provided a global checklist of fungi associated with this plant. Moreover, the information of fungi associated with Bidens pilosa was provided in previous studies (Abdou et al. 2010; Guatimosim et al. 2015; Zhang et al. 2018; Li et al. 2020; Htet et al. 2024). However, more knowledge is still needed about the diversity of fungi in Asteraceae plants to understand the fungi associated with this plant family. Moreover, the diversity of fungi in these two invasive weeds in Thailand is being further explored.

Roussoellaceae was introduced by Liu et al. (2014) based on morphology and LSU, ITS, tef1-α and rpb2 sequence data. Members of Roussoellaceae can be found as saprobes and human pathogens (Ahmed et al. 2014; Liu et al. 2014; Mapook et al. 2020; Hyde et al. 2023; Wu et al. 2023). Currently, there are 12 genera in Roussoellaceae, viz., Appendispora, Cytoplea, Elongatopedicellata, Immorrhia, Neoroussoella, Pararoussoella, Pseudoneoconiothyrium, Pseudoroussoella, Roussoella, Roussoellopsis, Setoarthopyrenia, and Xenoroussoella (Wijayawardene et al. 2022; Index Fungorum www.indexfungorum.org).

Neoroussoella was introduced by Liu et al. (2014) to accommodate a saprobic roussoella-like taxon with the type species N. bambusae. The sexual morphology of Neoroussoella is defined by immersed ascostromata beneath a clypeus or epidermis, appearing as black, dome-shaped, or flattened ovoid structures on the host surface. The asci are bitunicate and cylindrical, while the ascospores are brown or yellowish-brown, ellipsoidal to fusiform, and 2-celled, surrounded by a mucilaginous sheath (Liu et al. 2014). The asexual morphology of Neoroussoella is characterized by superficial or immersed pycnidia with annellidic, ampulliform, cylindrical conidiogenous cells, producing hyaline, pale brown, oblong to ellipsoidal conidia, each with two guttules (Liu et al. 2014; Jayasiri et al. 2019). Currently, there are 15 epithets listed in the Index Fungorum (www.indexfungorum.org), viz., Neoroussoella alishanensis, N. bambusae, N. clematidis, N. chiangmaiensis, N. entadae, N. fulvicomae, N. heveae, N. lenispora, N. leucaenae, N. lignicola, N. magnoliae, N. peltophora, N. sedimenticola, N. solani, and N. thailandica. Recent studies into the genus have been conducted by De Silva et al. (2022) and Hyde et al. (2023).

Pseudoroussoella was introduced by Mapook et al. (2020) based on morphology and LSU, SSU, ITS, tef1-α and rpb2 sequence data. The sexual morph of Pseudoroussoella species is characterized by globose to subglobose, dark brown to black ascomata with an ostiole, comprised of textura epidermoidea to textura angularis or textura intricata cells, with septate, trabeculate pseudoparaphyses, 8-spored, bitunicate, fissitunicate, cylindrical to clavate asci with a pedicel, and uniseriate, hyaline to pale brown, oval to ellipsoid, 1-septate ascospores bearing a gelatinous sheath (Mapook et al. 2020). Asexual morphs of Pseudoroussoella species are distinguished by solitary, superficial, uni-loculate, globose to obpyriform, pycnidial conidiomata with an ostiole, comprised of textura angularis cells, annellidic, ampulliform to oblong, hyaline and unbranched conidiogenous cells and pale brown to reddish brown, aseptate conidia with guttules (Mapook et al. 2020). Currently, two species are listed in the Index Fungorum (www.indexfungorum.org).

Some genera from Roussoellaceae, like Roussoella and Neoroussoella, are recognized for their bioactive secondary metabolites (Takekawa et al. 2013; Phukhamsakda et al. 2018; Chen et al. 2021; Zhong et al. 2021; Sommart et al. 2022). Moreover, the prescreening for antibacterial activity conducted by Mapook et al. (2020) revealed that Pseudoroussoella elaeicola (MFLUCC 17-1483) inhibits the growth of E. coli, resulting in a 10 mm inhibition zone. These findings showed that the species of Roussoellaceae are potential organisms for the production of bioactive secondary metabolites.

In this study, we introduce one new species of Pseudoroussoella on Bidens pilosa (Asteraceae), and one new species with a new host record of Neoroussoella on Chromolaena odorata (Asteraceae). We also provide an updated phylogenetic tree for Roussoellaceae, based on a combined dataset of LSU, SSU, ITS, tef1-α and rpb2 sequence data. Further, we explore the potential antibacterial activity of our three isolates and discuss their implications for future discoveries of bioactive compounds.

Materials and methods

Sample collection, morphological study and isolation

Dead stems from the Asteraceae plants, Bidens pilosa and Chromolaena odorata, were collected from northern Thailand. All specimens were brought to the lab in plastic bags labelled with the collection information. Single spore isolation was performed on malt extract agar (MEA) and incubated at 27 °C for 24 hours (Senanayake et al. 2020). The spores were germinated within 24 h using a Motic SMZ 168 Series microscope (Motic Asia, Hong Kong). Germinated spores were transferred to fresh MEA plates. All the detailed morphological characteristics were observed using a Nikon ECLIPSE 80i compound microscope (Nikon, Japan) fitted to a Canon 550D digital camera (Canon, Japan). Tarosoft Image Framework (v 0.9.7) was used to measure photomicrograph structures. Adobe Photoshop CS6 Extended (v 10.0.) was used to edit and prepare photo plates (Adobe system, USA). Forty-day-old cultures were used for molecular studies. Specimens were deposited at the Mae Fah Luang University Herbarium (Herb. MFLU) while living cultures were maintained at Mae Fah Luang University Culture Collection (MFLUCC). Faces of fungi (FoF) and Index Fungorum (IF) numbers were obtained as instructed by Jayasiri et al. (2015) and Index Fungorum (www.indexfungorum.org). Moreover, the species descriptions were submitted to the GMS Microfungi database (Chaiwan et al. 2021).

DNA extraction, PCR amplification and sequencing

Fifty-day-old fungal mycelium was scraped off and placed into a 1.5 ml micro-centrifuge tube using a sterile lancet. Genomic DNA extraction was done using the E.Z.N.A.® Tissue DNA Kit (Omega Biotek Inc., Georgia). Polymerase chain reaction (PCR) was used for DNA amplifications, following the protocols of Mapook et al. (2016). The details of PCR primers and protocols are shown in Table 1. The quality of PCR products was confirmed on 1% agarose gels. Purification and sequencing of PCR fragments with the primers mentioned above were carried out at a commercial sequencing provider (Solgent Co., Ltd, Thailand). The newly generated nucleotide sequences were deposited in the GenBank, and accession numbers were obtained (Table 2).

Table 1.
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PCR conditions used in this study.

Gene Primers PCR Conditions
Forward Reverse
Large subunit (LSU) LR0R LR5 95 °C: 3 min, (94 °C: 30 s, 56 °C: 50 s, 72 °C: 1 min) × 40 cycles 72 °C: 7 min.
Small subunit (SSU) NS1 NS4 95 °C: 3 min, (94 °C: 30 s, 55 °C: 50 s, 72 °C :1 min) × 40 cycles 72 °C: 7 min.
Internal transcribed spacer (ITS) ITS5 ITS4 95 °C: 3 min, (94 °C: 30 s, 55 °C: 50 s, 72 °C :1 min) × 40 cycles 72 °C: 7 min.
Elongation factor-1 alpha (tef1- α) EF1-983F EF1-2218R 95 °C: 3 min, (94 °C: 30 s, 55 °C: 50 s, 72 °C: 1 min) × 40 cycles 72 °C: 7 min.
RNA polymerase II subunit (rpb2) fRPB2-5F fRPB2-7cR 95 °C: 5 min, (95 °C : 1 min, 52 °C: 2 min, 72 °C: 90 s) × 40 cycles 72 °C: 10 min
Table 2.
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List of taxa, specimens and sequences used in phylogenetic analyses.

Species Strain numbers GenBank accession numbers
ITS LSU SSU tef1- α rpb2
Neoroussoella alishanense FU31016 MK503816 MK503822 MK503828 – MN037756
N. alishanense FU31018 MK503818 MK503824 MK503830 MK336182 MN037757
N. bambusae MFLUCC 11-0124 T KJ474827 KJ474839 – KJ474848 KJ474856
N. chromolaenae sp. nov. MFLUCC 24-0274 PQ226190 PQ226193 PQ226196 PQ240621 PQ240623
N. clematidis MFLUCC 17-2061 MT310632 MT214587 MT226700 MT394645 MT394701
N. entadae MFLUCC 18-0243 MK347786 MK348004 MK347893 MK360065 MK434866
N. entadae MFLUCC 24-0275 PQ226191 PQ226194 PQ226197 – PQ240624
N. fulvicomae MFLUCC 17-2073 MT310633 MT214588 MT226701 MT394646 MT394702
N. heveae MFLUCC 17-1983 MH590693 MH590689 MH590691 – –
N. lenispora GZCC 16-0020 T – KX791431 – – –
N. leucaenae MFLUCC 18-1544 MK347767 MK347984 MK347874 MK360067 MK434876
N. leucaenae MFLUCC 17-0927 MK347733 MK347950 MK347841 MK360066 MK434896
N. lignicola MUT 5008 MN556318 MN556320 MN556308 MN605895 MN605915
N. lignicola MUT 5373 KU314953 MN556321 KU314954 MN605896 MN605916
N. lignicola MUT 4904 KT699129 MN556319 MN556307 MN605894 MN605914
N. magnoliae MFLU 18-1022 MK801232 MK801230 MK801231 MK834373 –
N. peltophora MFLUCC 21-0071 MZ567051 MZ567206 MZ567207 MZ605441 MZ605442
N. sedimenticola CGMCC 3.22470 OQ798949 OQ758144 OQ809046 OQ809008
N. sedimenticola CGMCC 3.22468 T OQ798948 OQ758143 OQ809045 OQ809007
N. solani KT3264 T LC195218 LC195209 LC195206 LC195212 –
N. solani KT3265 T LC195219 LC195210 LC195207 LC195213 LC195216
N. thailandica MFLUCC 18-0721 OL703581 OL457704 OL764415 OM505028 ON502386
Occultibambusa bambusae MFLUCC 11-0394 KU940124 KU863113 – KU940194 KU940171
O. bambusae MFLUCC 13-0855 KU940123 KU863112 KU872116 KU940193 KU940170
Pseudoneoconiothyrium rosae MFLUCC 15-0052 T MG828922 MG829032 MG829138 – –
P. euonymi CBS 143426 T MH107915 MH107961 – – MH108007
P. euonymi GLMC 1544 MT153733 MT156304 – – –
Pseudoroussoella bidenticola sp. nov. MFLUCC 24-0273 PQ226192 PQ226195 PQ226198 PQ240622 PQ240625
Ps. chromolaenae MFLUCC 17-1492 T MT214345 MT214439 MT214393 MT235769 –
Ps. elaeicola MFLUCC 15-0276a T MT153733 MT156304 – – –
Ps. elaeicola MFLUCC 15-0276b MH742330 MH742327 – – –
Ps. elaeicola MFLUCC 17-1483 MT214348 MT214442 – MT235772 MT235808
Pararoussoella mangrovei MFLUCC 17-1542 MH025951 MH023318 – MH028246 –
P. mukdahanensi HKAS 101766 MH453489 MH453485 – MH453478 MH453482
P. rosarum MFLUCC 17-0796 T MG828939 MG829048 NG_061294 MG829224 MH028250
Roussoella arundinacea CPC 35554 MT223838 MT223928 – MT223723 –
R. bambusarum GMB0316(HT) ON479891 ON479892 – ON505015 ON505011
R. bambusarum GMB0390 ON505055 ON505051 – ON505017 ON505012
R. chiangraina MFLUCC 10-0556 T KJ474828 KJ474840 – KJ474849 KJ474857
R. doimaesalongensis MFLUCC 14-0584 T KY026584 KY000659 – KY651249 KY678394
R. hysterioides CBS 546.94 T KF443405 KF443381 AB524480 KF443399 KF443392
R. intermedia CBS 170.96 KF443407 KF443382 KF443390 KF443398 KF443394
R. japanensis MAFF 239636 T KJ474829 AB524621 – AB539114 AB539101
R. kunmingensis HKAS 101773 MH453491 MH453487 – MH453480 MH453484
R. margidorensis MUT 5329 T KU314944 MN556322 MN556309 MN605897 MN605917
R. mediterranea MUT 5306 KU255054 MN556323 MN556310 MN605898 MN605918
R. mexicana CPC25355 T KT950848 KT950862 – – –
R. neopustulans MFLUCC 11-0609 T KJ474833 KJ474841 – KJ474850 –
R. neopustulans MFLUCC 12-0003 T KU940130 KU863119 KU872122 – –
R. nitidula MFLUCC 11-0182 T KJ474835 KJ474843 – KJ474852 KJ474859
R. nitidula MFLUCC 11-0634 T KJ474834 KJ474842 – KJ474851 KJ474858
R. padinae MUT 5341 KU158153 MN556325 – MN605900 MN605920
R. padinae MUT 5365 KU158170 MN556326 KU158179 MN605901 MN605921
R. padinae MUT 5503 KU314993 MN556327 MN556312 MN605902 MN605922
R. pseudohysterioides MFLUCC 13-0852 T KU940131 KU863120 – KU940198 –
R. pustulans KT 1709 – AB524623 AB524482 AB539116 AB539103
R. scabrispora MFLUCC 11-0624 KJ474836 KJ474844 – KJ474853 KJ474860
R. siamensis GMB0317 ON4617749 ON461896 – ON505014 ON505010
R. siamensis GMB0391 ON505054 ON505053 – ON505018 ON505013
R. tosaensis KT 1659 – AB524625 AB524484 AB539117 AB539104
R. tuberculata MFLUCC 13-0854 T KU940132 KU863121 – – –
R. verrucispora CBS 125434 T KJ474832 – – – –
R. yunnanensis HKAS 101762 T MH453492 MH453488 – MH453481 –
R. yunnanensis MFLUCC 12-0005 T KJ739604 KJ474847 KJ739608 KJ474855 KJ474862
Xenoroussoella triseptata MFLUCC 17-1438 MT214343 MT214437 MT214391 MT235767 MT235804
X. triseptata KNUF-20-NI009 LC719282 LC719283 LC723530 LC723531 LC723532

* Remarks: The letter T denotes ex-type isolates. The newly generated sequences, new species and synonymized isolates are indicated in bold font.

Sequence alignment and phylogenetic analyses

Based on the sequence data of recent publications (De Silva et al. 2020; Li et al. 2023) and BLAST search results, reference taxa were selected, and phylogenetic analyses were conducted using the combined LSU, SSU, ITS, tef1-α and rpb2 sequence data. Sequence alignments were made with the MAFFT v. 7 online tool (http://mafft.cbrc.jp/alignment/server; 2016). Alignments were improved where necessary, and composite sequence alignments were obtained using MEGA v. 6.0.

RAxML and Bayesian analyses were carried out on the CIPRESS Science Gateway Portal (http://www.phylo.org) (Miller et al. 2010). Maximum likelihood analysis was performed by RAxML-HPC v.8 (Stamatakis 2014) with rapid bootstrap analysis, followed by 1000 bootstrap replicates and the GTRGAMMA substitution model. MrBayes was used to perform BI analysis on XSEDE 3.2.7 (Ronquist et al. 2012), with tree samples taken at every 1000th generation during the 5,000,000-generation run of four concurrent Markov chains. The first 25% of the trees were removed as part of the burn-in phase, and calculations for the Posterior Probability were made for the remaining 75% of the trees (PP) (Rannala and Yang 1996; Zhaxybayeva and Gogarten 2002). The phylogenetic tree was displayed using Fig. Tree v1.4.0 (Rambaut 2012) and was modified in Microsoft Office PowerPoint v. 2013.

Preliminary screening for antibacterial activity

Preliminary screening for antibacterial activity was carried out following the methods of Htet et al. (2024). Antibacterial discs of ampicillin were used as a positive control for screening (Alam et al. 2019). Antibacterial activity against gram positive bacteria (Bacillus subtilis-TISTR 1248 and Staphylococcus aureus-TISTR Y4b), and gram-negative bacteria (Escherichia coli TISTR 527) were investigated using the agar plug diffusion method (Balouiri et al. 2016). Bacteria test organisms were obtained from Scientific and Technological Instrument Center, Mae Fah Luang University. Bacterial test organisms were sub cultured and grown on Nutrient Agar (NA) for 24 hours. After 24 hours of inoculation, 2–3 loops of the bacterial test organisms were transferred to the nutrient broth and incubated for 24 hours in a shaking incubator. Prior to adding microbial suspensions to the sterile Mueller-Hinton agar media, cell counts were performed on the suspensions (6.7 × 105 cells/mL), as detailed by Mapook et al. (2020). Fungal mycelium plugs from our isolates were transferred to a solid medium plate and allowed to grow at room temperature for 24–48 hours. Inhibition zones were measured and compared to the positive control.

Results

Phylogenetic analyses

The combined LSU, SSU, ITS tef1-α, and rpb2 sequence dataset comprises 66 taxa with Occultibambusa bambusae strains (MFLUC 13-0855 and MFLUCC 11-0394) as the outgroup taxa. Maximum likelihood (ML) analyses and Bayesian Inference (BI) of the combined dataset were performed to determine the placement of our new isolates. Tree topologies of ML and BI criteria were similar to earlier investigations (De Silva et al. 2020; Li et al. 2023). The best-scoring RAxML tree with a final likelihood value of -28736.822321 is shown in Fig. 1. RAxML analysis yielded 1578 distinct alignment patterns, with 29.39% of undetermined characters or gaps. Estimated base frequencies were as follows: A = 0.245746, C = 0.258383, G = 0.266559, T = 0.229312; substitution rates: AC = 1.714222, AG = 4.957697, AT = 1.884927, CG = 1.345111, CT = 9.562411, GT = 1.000000; gamma distribution shape parameter α = 0.166563. In our phylogenetic analysis, Neoroussoella chromolaenae sp. nov. (MFLUCC 24-0274) clustered with Neoroussoella entadae (MFLUCC 18-0243 and MFLUCC 24-0275) with 100% ML and 1.00 BYPP support. Furthermore, our isolate, Pseudoroussoella bidenticola sp. nov. (MFLUCC 24-0273) formed a branch separated from Ps. elaeicola (MFLUCC 17-1483, MFLUCC 15-0276a, MFLUCC 15-0276b), and Ps. chromolaenae (MFLUCC 17-1492) with 96% ML and 1.00 BYPP, respectively.

Figure 1. 

Phylogram generated from maximum likelihood analysis based on the combined dataset of LSU, SSU, ITS, tef1-α and rpb2 sequence data. Bootstrap support values for ML equal to or greater than 75% and BYPP equal to or greater than 0.90 are given at the nodes. Newly generated sequences are in blue and type species are in bold.

Taxonomy

Neoroussoella chromolaenae Z.H. Htet, A. Mapook & K. D. Hyde, sp. nov.

Index Fungorum: IF902613
Facesoffungi Number: FoF16402
Fig. 2

Etymology

Name reflects the host plant Chromolaena odorata, from which this species was isolated.

Holotype

MFLU 24-0264.

Description

Saprobic on the dead stems of Chromolaena odorata (Asteraceae). Sexual morph: Undetermined. Asexual morph: Coelomycetous. Conidiomata 70–150 × 120–150 µm (av. 85 × 138 µm, n = 5), pycnidial, solitary, uniloculate, immersed, ostiolate. Ostiole papillate. Peridium 10–20 µm wide, comprising 2–3 layers of brown cells of textura angularis. Conidiophores reduced to conidiogenous cells. Conidiogenous cells 3–5 × 2–3.5 µm (av. 3 × 3 µm, n = 10), phialidic, ampulliform to cylindrical, hyaline. Conidia 3–6 × 2–4 μm (av. 4.4 × 3.1 μm, n = 20), hyaline, oblong to slightly ellipsoid, aseptate, with small guttules.

Culture characteristics

Conidia germinating on MEA within 24 hours, reaching 22 mm after 10 days at 27 °C, irregular, curled margin, brown in the middle and becoming pale brown on the outer parts of the culture, wrinkled on the surface; wrinkle, pale brown to brown in reverse.

Figure 2. 

Neoroussoella chromolaenae (MFLU 24-0264, holotype) a, b Conidiomata on the substrate c a section through conidioma d ostiole e peridium f conidia and conidiogenous cells g–i conidia j germinating conidia k culture on the MEA. Scale bars: 500 µm (a, b); 100 µm (c); 20 µm (d, e); 10 µm (e–j).

Material examined

Thailand • Chiang Rai Province, Doi Pui, 19°48'51"N, 99°52'1"E, on dead stems of Chromolaena odorata (Asteraceae), 14 March 2023, Zin Hnin Htet (CO-DP-3, MFLU 24-0264, holotype); ex-type culture MFLUCC 24-0274.

Notes

In a megablast search of GenBank, the closest match for the ITS sequence of our isolate was fungal sp. isolate NFC-3 (MG189955) with 99.47% similarity. The closest match for the LSU region was N. solani CBS 141288 (MH878207) with 100% similarity, and the closest match for the SSU region was N. bambusae strain GMB1295 (OM764650) with 93.99% similarity. Additionally, the closet matches for the tef1-α and rpb2 gene regions were Neoroussoella entadae strain MFLUCC 18-0243 (MK360065) and N. entadae strain MFLUCC 17-0920 (MK434898) with 99.45% and 99.77% similarities, respectively.

Based on the multi-locus phylogeny (Fig. 1), our isolate (MFLUCC 24-0274) formed a separate branch from N. entadae with 100% ML and 1.00 BYPP. A comparative analysis of base pair differences between Neoroussoella chromolaenae (MFLUCC 24-0274) and Neoroussoella entadae (MFLUCC 18-0243) revealed variations in ITS (0.6% - 3/476), LSU (0.1% - 1/838), SSU (1.9% - 14/717), tef1-α (0.5% - 5/902), and rpb2 (2.0% - 18/885) without gaps, respectively. Morphologically, our collection is similar to N. entadae (MFLUCC 17–0920) in having solitary, unilocular, ostiolate, phialidic, ampulliform to cylindrical, hyaline conidiogenous cells, and oblong to ellipsoidal, hyaline conidia (Jayasiri et al. 2019). However, our species differs from N. entadae (MFLUCC 17–0920) in having smaller conidiomata (70–150 × 120–150 µm vs. 127–192 × 161–190 µm), slightly wider conidiogenous cells (2–3.5 µm vs. 0.7–1.8 µm) and larger conidia size (3–6 × 2–4 μm vs. 3–4 × 1.7–1.9 μm). Therefore, N. chromolaenae is described here as a new species based on phylogeny and morphological evidence. Synopsis of the asexual morph of Neoroussoella species is also provided in Table 3.

Table 3.
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Synopsis of asexual morph species in Neoroussoella.

Species Conidiomata (µm) Conidiogenous cells (µm) Conidia (µm) References
Neoroussoella alishanense (FU31016) 130–140, 210–225 8–14 × 2–3 3–4 × 2–3 Karunarathna et al. (2019)
Neoroussoella bambusae (MFLUCC 11-0124) 200–430 × 300–420 8–13.5 × 1.5–3 3–4 × 1.5–2 Liu et al. (2014)
Neoroussoella chromolaenae (MFLUCC 24-0274) 70–150 × 120–150 3–5 × 2–3.5 3–6 × 2–4 This study
Neoroussoella entadae (MFLUCC 17–0920) 127–192 × 161–190 3.5–5.6 × 0.7–1.8 3–4 × 1.7–1.9 Jayasiri et al. (2019)
Neoroussoella entadae (MFLUCC 24-0275) 70–120 × 100–150 3–5 × 1–3 3–5 × 2–4 This study
Neoroussoella heveae (MFLUCC 17-0338) 90–130, 115–180 3–7 × 2–5 2.5–5 × 2–4 Phookamsak et al. (2019)
Neoroussoella leucaenae (MFLUCC 18–1544) 135–175 × 120–180 5.5–9 × 3–4 3.5–4.5 × 1.9–2.6 Jayasiri et al. (2019)
Neoroussoella peltophora (MFLUCC 21-0071) 165–224 × 144–178 1–3.5 × 6.5–8 2.0–3.0 × 3.0–4.0 Pasouvang et al. (2022)
Neoroussoella solani (CPC 26331) To 150 4–6 × 3–4 4.5–5 × 2–3 Crous et al. (2016)

Neoroussoella entadae Jayasiri, E.B.G. Jones & K.D. Hyde, Mycosphere 10(1): 105 (2019)

Index Fungorum: IF555568
Facesoffungi Number: FoF05275
Fig. 3

Description

Saprobic on the dead stems of Chromolaena odorata (Asteraceae). Sexual morph: Undetermined. Asexual morph: Coelomycetous. Conidiomata 70–120 × 100–150 µm (av. 95 × 110 µm, n = 5), pycnidial, solitary, globose to subglobose, uniloculate, immersed to semi-immersed, ostiolate. Ostiole 30–35 µm wide, with small papillate. Peridium 10–20 µm wide, comprising 2–3 layers of brown cells of textura angularis. Conidiophores reduced to conidiogenous cells. Conidiogenous cells 3–5 × 1–3 µm (av. 3.8 × 2.1 µm, n = 10), phialidic, ampulliform to cylindrical, hyaline. Conidia 3–5 × 2–4 μm (av. 3.8 × 2 μm, n = 20), hyaline, becoming pale brown when gathering, oblong to ovoid, aseptate, with small guttules.

Culture characteristics

Conidia germinating on PDA within 24 hours, reaching 24 mm after 7 days at 27 °C, irregular, entire, yellowish-brown, slightly wrinkled on the surface; pale brown to brown in reverse.

Figure 3. 

Neoroussoella entadae (MFLU 24-0265, new host record) a, b Conidiomata on the substrate c a section through conidioma d ostiole e peridium f conidia and conidiogenous cells g–i conidia j a germinating conidium k culture on the MEA. Scale bars: 500 µm (a); 200 µm (b); 50 µm (c); 20 µm (d, e); 5 µm (f, g, h, i, j).

Material examined

Thailand • Chiang Rai Province, Thoeng district, on dead stems of Chromolaena odorata (Asteraceae), 24 Jan 2022, A. Mapook (TCR18, MFLU 24-0265, new host record); living culture MFLUCC 24-0275.

Known host distribution

Entada phaseoloides (Fabaceae), Leucaena sp. (Fabaceae) (Jayasiri et al. 2019).

Notes

In a BLASTn search of GenBank, the closest match for the ITS sequence of our isolate was N. solani strain MnF107 (OQ704272) with 99.83% similarity. The closest match for the LSU region was Roussoella sp. strain HF3S53 (OP179275) with 99.77% similarity, and the closest match for the SSU region was Pleosporales sp. IRB20-2 (AB195632) with 100% similarity. The closest match for the tef1-α and rpb2 gene region was Neoroussoella entadae strain MFLUCC 18-0243 (MK434866) with 99.78% and 99.53% similarity, respectively.

When we compared the morphology, our isolate is similar to N. entadae (MFLUCC 17–0920) in having solitary, unilocular, ostiolate conidiomata, phialidic, ampulliform to cylindrical, hyaline conidiogenous cells, and oblong to ovoid, hyaline conidia with size (3–5 × 2–4 μm vs 3–4 × 1.7–1.9 μm). However, our isolate differs from N. entadae (MFLUCC 17–0920) in having smaller conidiomata (70–120 × 100–150 µm vs. 127–192 × 161–190 µm), slightly wider conidiogenous cells (3–5 × 1–3 µm vs. 3.5–5.6 × 0.7–1.8 µm) (Table 3).

Based on the multi-locus phylogeny (Fig. 1), our isolate MFLUCC 24-0275 clustered in the same clade with N. entadae (MFLUCC 18-0243). Moreover, there is no significant base pair difference between MFLUCC 24-0275 and N. entadae (MFLUCC 18-0243). Therefore, we reported N. entadae as the first occurrence on C. odorata (Asteraceae) based on morphology and multigene phylogeny.

Pseudoroussoella bidenticola Z.H. Htet, A. Mapook & K. D. Hyde, sp. nov.

Index Fungorum: IF902614
Facesoffungi Number: FoF16403
Fig. 4

Etymology

Name reflects the host plant Bidens pilosa, from which this species was isolated.

Holotype

MFLU 24-0266.

Description

Saprobic on dead stems of Bidens pilosa. Sexual morph: Undetermined. Asexual morph: Coelomycetous. Conidiomata 120–150 × 150–180 µm (av. 126 × 173 µm, n = 5), pycnidial, solitary, immersed to semi-immersed, uni-loculate, brown, globose to subglobose, dark fruiting bodies on the host substrate, without an ostiole. Peridium 10–20 µm wide, comprising 2–3 layers of yellowish brown to brown cells of textura angularis. Conidiophores reduced to conidiogenous cells. Conidiogenous cells 1–2 μm long, holoblastic, short, globose to subglobose, hyaline and unbranched. Conidia 5–7.5 × 4–5.5 μm (av. 6 × 4.8 µm, n = 20), globose to subglobose, brown to reddish brown, aseptate, thick-walled with a guttule.

Figure 4. 

Pseudoroussoella bidenticola (MFLU 24-0266, holotype) a, b Conidiomata on the substrate c a section through a conidioma d peridium e conidia and conidiogenous cell f–i conidia j germinating conidia k culture on the MEA. Scale bars: 500 µm (a, b); 100 µm (c); 10 µm (d); 5 µm (e–i).

Culture characteristics

Conidia germinating on MEA within 24 hours, reaching 27 mm after 10 days at 27 °C, irregular, entire, concentric, opaque, flat, white to pale brown on the surface; concentric, creamy to pale brown in reverse.

Material examined

Thailand • Chiang Rai Province, Doi Pui, 19°48'51"N, 99°52'1"E, on dead stems of Bidens pilosa (Asteraceae), 14 March 2023, Zin Hnin Htet (BP-DP-11, MFLU 24-0266, holotype); ex-type culture MFLUCC 24-0273.

Notes

In a BLASTn search of GenBank, the closest match for the ITS sequence of our isolate was Roussoella elaeicola strain MFLUCC 15-0276b (MH742330) with 94.57% similarity. The closest match for the LSU region was Pseudoroussoella chromolaenae isolate MFLUCC 17-2062 (MT394704) with 92.95% similarity, and the closest match for the SSU region was Parathyridaria tyrrhenica MUT<ITA>:5371 (KU314952) with 99.16% similarity. Additionally, the closest matches for the tef1-α and rpb2 gene regions were Pseudoroussoella elaeicola culture MFLUCC:17-1483 (MT235772) and Roussoella sp. strain GMB1153 (OM755588) with 97.08% and 98.27% similarity, respectively.

Pseudoroussoella elaeicola (MFLUCC 17-1483 and MFLUCC 17–2086) was found as a sexual morph in nature (Phookamsak et al. 2019, Mapook et al. 2020); hence, we were unable to directly compare their morphology with our isolate. However, based on comparing the morphology of Pseudorousoella bidenticola (MFLUCC 24-0273) and Ps. chromolaenae (MFLUCC 17-1492), our species differs from Ps. chromolaenae (MFLUCC 17-1492) in having immersed to semi-immersed, globose to subglobose, brown, conidiomata without ostiole, smaller-sized (120–150 × 150–180 µm vs 130–175(–230) × 160–230 µm), holoblastic, globose to subglobose conidiogenous cells, and brown to reddish brown, globose to subglobose conidia with guttules, while Ps. chromolaenae (MFLUCC 17-1492) displays superficial, globose to obpyriform, yellowish brown to brown conidiomata with a central ostiole, annellidic, ampulliform to oblong conidiogenous cells, and oblong to oval, conidia that are pale brown to light brown when immature, becoming yellowish brown to reddish brown when mature (Table 4).

Table 4.
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Synopsis of sexual and asexual morph of Chromolaenicola species.

Species Conidiomata (µm) Conidiogenous cells (µm) Conidia (µm) References
Pseudoroussoella chromolaenae (MFLUCC 17-1492) 130–175(–230) × 160–230 – 5.5–7 × 3.5–5 Mapook et al. (2020)
Pseudoroussoella bidenticola (MFLUCC 24-0273) 120–150 × 150–180 1–2 5–7.5 × 4–5.5 This study
Species Ascomata (µm) Asci (µm) Ascospores (µm) References
Pseudoroussoella elaeicola 225–475 × 240–400 95–135 × 6–8.5 10–14 × 4.5–6 Mapook et al. (2020)

Based on the multi-locus phylogeny (Fig. 1), our isolate (MFLUCC 24-0273) formed a separate branch related to Pseudoroussoella species with 96% ML and 1.00 BYPP. When comparing base pair differences between Ps. bidenticola (MFLUCC 24-0273) and Ps. chromolaenae (MFLUCC 17-1492), variations were observed in ITS (3.6% - 23/469), LSU (0.6% - 5/799), SSU (0.6% - 4/630), tef1-α (2.6% - 24/891), without gaps. Therefore, we introduced our collection (MFLUCC 24-0273) as a new species based on morphology and multigene phylogeny. Moreover, this is also the first record of Pseudoroussoella species from Bidens pilosa (Asteraceae).

Preliminary screening for antibacterial activity

In our study, we explored the antibacterial activities of our three isolates against Bacillus subtilis, Escherichia coli coli, and Staphylococcus aureus. Neoroussoella chromolaenae (MFLUCC 24-0274), N. endatae (MFLUCC 24-0275), Pseudoroussoella bidenticola (MFLUCC 24-0273) exhibited antibacterial activity against all three test organisms. For B. subtilis, N. chromolaenae (MFLUCC 24-0274), N. entadae (MFLUCC 24-0275), and Ps. bidenticola (MFLUCC 24-0273) exhibited partial inhibition. Against E. coli, N. chromolaenae (MFLUCC 24-0274), N. entadae (MFLUCC 24-0275), and Ps. bidenticola (MFLUCC 24-0273) demonstrated clear inhibition. For S. aureus, N. chromolaenae (MFLUCC 24-0274) showed the most significant inhibition, followed by N. entadae (MFLUCC 24-0275) and Ps. bidenticola (MFLUCC 24-0273), with clear inhibition observed. However, none of these fungal species showed a wider inhibition zone than the positive control, ampicillin (20 mm for B. subtilis, 50 mm for E. coli, 40 mm for S. aureus). The measurements of clear inhibition zones produced by our new isolates are provided in Table 5.

Table 5.
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Preliminary antibacterial activity result of this study.

Species Zone of inhibition (mm); Ampicillin (+)
Bacillus subtilis Escherichia coli Staphylococcus aureus
Neoroussoella chromolaenae (MFLUCC 24-0274) 16 mm inhibition 11 mm inhibition 20 mm inhibition
N. entadae (MFLUCC 24-0275) 13 mm inhibition 17 mm inhibition 14 mm inhibition
Pseudoroussoella bidenticola (MFLUCC 24-0273) 18 mm inhibition 12 mm inhibition 13 mm inhibition

Abbreviation: Positive control (+).

Discussion

Our research in northern Thailand unveiled the introduction of two novel species and one new host record within the Roussoellaceae. This classification was determined through a combination of morphological analyses and a multigene phylogeny approach, adhering to the recommendations outlined by Jeewon and Hyde(2016). Mapook et al. (2020) established Pseudoroussoella to accommodate Ps. chromolaenae and Ps. elaeicola. Interestingly, our study revealed a third Pseudoroussoella strain on the dead stems of Bidens pilosa (Asteraceae). In our phylogenetic analyses, our isolate (MFLUCC 24-0273) formed a basal lineage to other strains (MFLUCC 17-1483; MFLUCC 15-0276a; MFLUCC 15-0276b and MFLUCC 17-1492). Our species is morphologically similar to Ps. chromolaenae and has a significant base pairs difference between the two, and herein, we introduced our isolate as a new species. Moreover, we found two isolates of Neoroussoella on the dead stems of C. odorata (Asteraceae). Based on the morphological similarity and multigene phylogeny, we identified N. chromolaenae as a new species and N. entadae as the first occurrence on Chromolaena odorata.

Following the preliminary screening for antibacterial activity, all species examined in our study demonstrated potential antibacterial properties. In a prior examination of Pseudoroussoella species, Ps. chromolaena exhibited no inhibition on B. subtilis, E. coli, and M. plumbeus, while Ps. elaeicola displayed a 10 mm inhibition zone against E. coli (Mapook et al. 2020). Our isolate (MFLUCC 24-0273) exhibited inhibition on all tested organisms, with inhibition zones measuring 18 mm (B. subtilis), 12 mm (E. coli), and 13 mm (S. aureus), respectively. These results highlight our new species, Pseodoroussoella bidenticola, as a particularly promising organism for further research. Additionally, Neoroussoella chromolaenae (MFLUCC 24-0274) and N. entadae (MFLUCC 24-0275) demonstrated inhibitory effects against all test organisms, and specific measurements of inhibition zones are shown in Table 4. Across the three observed species, all species exhibited antibacterial activity. The outcomes of our investigation suggest that this fungal group possesses antibacterial potential, presenting a source for the exploration of novel bioactive compounds. These findings also highlight the potential of the Roussoellaceae family for antibacterial compound discovery, a field that remains relatively underexplored.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

This research was funded by the Basic Research Fund support from the National Science, Research and Innovation Fund (Grant No. 652A01001, 662A01001 and 672A16001) entitled “Studies of fungi associated with Asteraceae and the discovery of biological properties”, Mae Fah Luang University Grant - Reinventing University System (Grant No. 652A16049), Distinguished Scientist Fellowship Program (DSFP), King Saud University, Kingdom of Saudi Arabia.

Author contributions

The authors confirm contributions to the paper as follows: Fungal specimen collection and isolation, fungal specimen deposition and manuscript writing: Zin Hnin Htet; fungal identification and contributed in the revision of the manuscript: Zin Hnin Htet, Kevin D. Hyde, Fatimah O. Alotibi, Ausana Mapook, Thilini K. W. Chethana. All authors have read and agreed to the published version of the manuscript. All authors reviewed the results and approved the final version of the manuscript.

Author ORCIDs

Zin Hnin Htet https://orcid.org/0000-0002-6652-6975

Kevin D. Hyde https://orcid.org/0000-0002-2191-0762

Fatimah O. Alotibi https://orcid.org/0000-0003-3629-5755

Thilini K. W. Chethana https://orcid.org/0000-0002-5816-9269

Ausana Mapook https://orcid.org/0000-0001-7929-2429

Data availability

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

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