Trichoderma juruarense sp. nov. (Hypocreaceae) a new fungal species from sediments of the Amazonian Juruá River with agricultural potential

doi:10.21203/rs.3.rs-1214667/v1

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Trichoderma juruarense sp. nov. (Hypocreaceae) a new fungal species from sediments of the Amazonian Juruá River with agricultural potential

https://doi.org/10.21203/rs.3.rs-1214667/v1

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The species of Trichoderma are the most common fungi to be used as biocontrol agents, and their metabolic arsenal has a wide variety of applications that places this genus among those with the potential to provide biotechnological products. The ubiquitous nature of Trichoderma has favored a rapid increase in the number of described species, and significant efforts have been made towards the taxonomy of Trichoderma in order to improve the accuracy of identification. During a study of cultivable microbiota from the Juruá River, Amazon, Brazil. Isolates with morphological characteristics of the genus Trichoderma were screened for their capacity to control phytopathogens. A total of five Trichoderma isolates were identified using morphological data combined with phylogenetic analysis of the ITS region, and partial sequences of TEF and RPB2. Trichoderma juruarense sp. nov. form a monophyletic clade that is closely related to T. cyanodichotomus, a species that occupies an unresolved position in the Trichoderma taxonomy. T. cyanodichotomus and T. juruarense sp. nov. present an intracellular blue-green pigment in potato dextrose agar (PDA) and differ in conidia and chlamydospores sizes. These data support the proposition of a new species, named here as Trichoderma juruarense. The holotype of T. juruarense INPA0108 presents in vitro inhibition against phytopathogens, such as Colletotrichum siamense (50%), Corynespora cassiicola (43%), Fusarium decemcellulare (61%) and Sclerotium rolfsii (51%), which demonstrates desirable traits that warrant further studies on plant protection. In addition, T. cyanodichotomus and T. juruarense formed a new clade based on the sequence data of the RPB2 gene.

Biological control

taxonomy

freshwater fungi

new taxon

The abundant biodiversity of the Amazon region is scattered among many distinct environments (upland forest, white-sand savanna, flooded forest, and floodplains). In this scenario, the high precipitation rate favors the deposition and transport of biological material along its flow, making the Amazonian wetlands a valuable source of biodiversity (Junk et al. 2010).

The Juruá River begins in Peru and flows for over 3,280 km inside the Brazilian territory, and is considered the world’s most sinuous river. Along the extension of the Juruá River, there are two environmental protection areas (Uacari Sustainable Development Reserve and the Medio Juruá Extractive Reserve) that host diverse ecosystems. Moreover, several indigenous communities live in this region, which is considered a promising place for the establishment of a circular economy, due to a highly diverse natural resource-based economy and strong social organization of local communities(da Silva Abel et al. 2021; Paes et al. 2021).

The Juruá River is the third largest whitewater tributary of the Amazon River and plays an important role in riverside communities, hosting a diverse inventory of fauna and flora species (Del-Rio et al. 2021). Annually, the Juruá River has a flood and ebb period (Colwell 2000), each one taking several months to complete. This phenomenon, also known as flood pulse (Junk et al. 1989), has a direct impact on the local economy, since agriculture, fishing and transportation are all directly influenced by the water level. Inundation of the floodplains along the Juruá River favors many ecological processes, including the exchange of genetically diverse biological material across distinct environments, which is especially favorable for microorganisms.

Within the microbial diversity of the Amazon region, several new species of Trichoderma have been identified, such as Trichoderma stromaticum (Samuels et al. 2000), Trichoderma ovalisporum (Holmes et al. 2004), Trichoderma theobromicola, T. paucisporum (Samuels et al. 2006b), Trichoderma martiale (Hanada et al. 2008, 2009), T. amazonicum (Chaverri et al. 2011), T. strigosellum (López-Quintero et al. 2013), T. awajun, T. jaklitschii and T. peruvianum (Bustamante et al. 2021). Despite all the Trichoderma species listed above originating from the Amazon biome, only T. stromaticum, T. ovalisporum and T. martiale were collected in Brazil, pointing to a gap in information regarding the diversity of Trichoderma in the Brazilian Amazon.

Trichoderma has been largely associated with enzyme production, plant protection and growth promotion, but the importance of this genera goes far beyond this, due to the vast amount of possible applications in agriculture and industry in the form of bioremediation, industrial enzymes, food additives, probiotics, antibiotics, pigments, biofuel production and battery components (Kunamneni et al. 2014; Kalsoom et al. 2019; Li et al. 2019, 2021; Shen et al. 2019; Daccò et al. 2020; Ghosh et al. 2020; Venil et al. 2020). Since some Trichoderma species can cause losses in mushroom production and infections in immunocompromised humans (Kredics et al. 2021), this makes an accurate species identification particularly important.

The taxonomy of Trichoderma has a long history of changes that were instigated by taxonomists who played a crucial role in the development and enhancement of the identification methods of Trichoderma. The genus was first introduced more than 200 years ago by Persoon in 1794 (Druzhinina et al. 2006). In 1966, the taxonomy of Trichoderma was reviewed based on the species’ life cycle (Rifai and Webster 1966), and the taxonomy of Trichoderma species was re-shaped (Druzhinina et al. 2006). Rifai revised the genus and proposed nine aggregated species (Rifai 1969) that were later redefined in sections by Bissett (Bissett 1984, 1991a, b, c), which differentiated new Trichoderma species within sections, and established 9 aggregates disposed into 4 sections based on morphological traits, resulting in 27 Trichoderma species. Less than a decade later. Subsequently, (Kindermann et al. 1998) presented the first ITS-based phylogeny of the whole genus. The first multigene phylogeny was ITS1, ITS2, TEF and ECH42, (Kullnig-Gradinger et al. 2002), which increased the number of species to 47.

Despite the advances in the identification of Trichoderma, the first steps into the “molecular era” revealed the lack of more strict quality control and standardization procedures during species identification, which favored the deposition of sequences with unreliable information. In 2005, the first attempt to standardize the identification of Trichoderma was made with the development of an automated method called TrichOKey (Druzhinina and Kubicek 2005; Druzhinina et al. 2005), which is considered the first fungal barcode for Trichoderma species, and is based on ITS1 and ITS2 regions. The low resolution of ITS regions for supporting species differentiation led to the development of a more robust method for the identification of Trichoderma, in which the most commonly used phylogenetic markers were added. This method is known as TrichoBLAST (Kopchinskiy et al. 2005).

A decade later, the taxonomy of T. harzianum species complex was revised and the identity of commercial strains of T. harzianum was determined (Chaverri et al. 2015) pointing out the low resolution of nuclear internal transcribed spacers rDNA regions for Trichoderma species delimitation. The mentioned study proposed the adoption of the translation elongation factor 1-α (TEF), as a more precise secondary barcode for Trichoderma species identification. Also in 2015, a list of 254 accepted names for Trichoderma species was published (Bissett et al. 2015). Recently, in an effort to standardize taxonomy procedures for Trichoderma, a guideline on molecular identification of Trichoderma was published that highlighted the difficulties involved in molecular identification of species from this genus (Cai and Druzhinina 2021).

The development of molecular methods for identification of Trichoderma changed the criteria for species delimitation and favored the exponential growth in the number of species. However, accurate molecular identification of Trichoderma species can be a challenging process even for experts, and sometimes leads to incorrect species identification (Cai and Druzhinina 2021). Inaccurately identified species can become a source for further misidentification, perpetuating this taxonomical issue. The genus Trichoderma presents several invalid species names due to lack of compliance with “The International Code of Nomenclature for algae, fungi, and plants” (Turland et al. 2018) or incomplete deposition in public databases (May et al. 2019). One example is Trichoderma cyanodichotomus strain TW21990_1, a potential biocontrol agent that is capable of promoting plant growth (Li et al. 2018; Zhou et al. 2020). Despite its description and available genomic data in public repositories, T. cyanodichotomus is still considered an illegitimate name due to failure to comply with all rules of the International Code of Nomenclature for algae, fungi, and plants. T. cyanodichotomus was first isolated from sediments from across the Pacific Ocean at Dongting Lake, China, and presented the production of a blue-green pigment as a striking feature. Moreover, the strain TW21990_1, showed production of enzymes of industrial interest, such as cellulase, β-1,3-glucanase, chitinase and protease.

The present study revealed a new species that forms a monophyletic clade with T. cyanodichotomus, strain TW21990_1, named here as T. juruarense and identified using morphological characters such as conidia, phialide and chlamydospore size combined with phylogenetic inference of RPB2 and TEF genes.

Trichoderma isolation from sediment collection

Trichoderma species were isolated from sediment samples collected along the Juruá River at the following coordinates: INPA 0105 and INPA 0106 (06° 44’ 45.1” S, 070° 07’ 35.0” W), INPA 0108 (06° 45’ 58.8” S, 070° 26’ 13.8” W), INPA 0111 (06° 49’ 32.8” S, 070° 40’ 59.5” W) and INPA 0149 (06° 33’ 18.6” S, 068° 59’ 22.9” W). The isolation was performed with standard procedures (Siddiquee 2017). The monosporic cultures were prepared using serial dilution; 300 µL of sterile water was placed in a sporulating plate, 100 µL of the conidia suspension was added to 900 µL of sterile water and used for serial dilution until 10⁻⁷. The last dilution was streaked onto water agar and a single colony was transferred to a new PDA plate.

Morphological evaluation

The morphological appearance was evaluated in potato dextrose agar (PDA), cornmeal dextrose agar (CMA) and synthetic low nutrient agar (SNA) media (Montoya et al. 2016) to determine the presence of pigments, autolytic activity, concentric rings, mycelium density and appearance, and conidiation color. Microstructures were evaluated using coverslip observation under a microscope (Carl ZEISS Axio Imager v2). The coverslips were previously placed in Petri dishes containing PDA medium. After inoculation, plates with coverslips were incubated for 4 days at 25 °C with photoperiod of 12:12 h light-dark, and observed under a microscope. Measurements were based on 50 sampled units of the following structures: chlamydospores, microconidia, macroconidia, and phialides (Table 1).

Morphological structures were also evaluated using scanning electron microscopy (SEM). Culture plugs were fixed with Karnovsky’s solution, rinsed with sodium cacodylate (0.1 M) for 20 min, post-fixed in osmium tetroxide for 40 min, dehydrated in ethanol series of different concentrations (20%, 30%, 50%, 70%, 90% and 95%), critical point dried, mounted in metal stubs, sputtered with gold and analyzed using conventional and field emission scanning electron microscopy (JSM-IT500HR InTouchScope™, Jeol).

DNA Extraction and Sequencing

DNA extraction followed the CTAB 2% method (Doyle and Doyle 1987) using mycelium grown in potato dextrose broth (PDB) for 4 days at 28 °C under 125 rpm. The DNA concentration was measured using spectrometry (NanoDrop1000) and the integrity was visualized on agarose gel (0.8%). The PCR reactions for the amplification of the ITS region and partial sequences of TEF and RPB2 were prepared using an Easytaq kit (Synapse Biotechnology) with three paired primers: ITS1 (TCCGTAGGTGAACCTGCGG) and ITS4 (TCCTCCGCTTATTGATATG), which amplifies 550 bp corresponding to the internal transcribed spacer I, 5,8 rDNA and internal transcribed spacer II (White et al. 1990), fRPB2-5f (GAYGAYMGWGATCAYTTYGG) and fRPB2-7cr (CCCATRGCTbTGTYYY), which amplifies 800 bp corresponding to the partial sequence of second largest subunit of RNA polymerase II (Liu et al. 1999), and EF-1αF (ATGGGTAAGGARGACAAGAC) and EF-1αR (GGARGTACCAGTSATCATGTT) primers, which amplifies 500 bp corresponding to the partial sequence of the translation elongation factor gene (O’Donnell et al. 1998; Carbone and Kohn 1999).

The PCR condition for amplification of all loci was initial denaturation at 95 °C for 3 min., 35 cycles of denaturation at 95 °C for 45 sec., annealing at a temperature of 55 °C for 45 sec., extension at 72 °C for 1 min., and final extension at 72°C for 5 min. The PCR products were resolved in agarose gel (1.5%) for confirmation of amplicon length using the 1 kb marker (Invitrogen). The PCR purification was carried out using exoSAP-IT (ThermoFisher; catalog number: 78200.200.UL), according to the manufacturer’s recommendations. The sequencing reactions were performed in a volume of 10 µL, containing 2 µL of ultrapure water, 1.5 µL of BigDye buffer, 0.5 µL of BigDye terminator v3.1 (Thermo Fisher), 1 µL of each primer and 5 µL of the purified PCR products. The cycling conditions were 96 °C for 1 minute, followed by 35 cycles at 96 °C for 15 seconds, 50 °C for 15 seconds, and 60 °C for 4 minutes. The sequencing was performed using a genetic analyzer (3500, Thermo Fisher).

Phylogenetic analyses

Consensus sequences of the ITS region and partial gene sequences of TEF and RPB2 were obtained manually based on the alignment of forward and reverse sequences as well as electropherogram analysis. The obtained sequences were deposited in Genbank under accession numbers OL639119-OL639123 (ITS), OL782574-OL782578 (TEF) and OL782579-OL782583 (RPB2).

The ITS sequences were used to confirm the genus as previously determined by morphological traits. For the identification of the isolates INPA 0105, INPA 0106, INPA 0108, INPA 0111 and INPA 0149 at species level, a dataset based on the concatenation of partial sequences of the genes TEF and RPB2 of closely related species observed in previous phylogenetic inference totaled 36 species of Trichoderma of clade I, 11 species of clade II and 5 species of clade IV, in addition to Arachnocrea scabrida, which was used as an outgroup (Table 2). The sequences were aligned in the MAFFT online platform (https://mafft.cbrc.jp/alignment/software/) and submitted to maximum-likelihood (ML) analysis in IQ-TREE (Nguyen et al. 2015; Chernomor et al. 2016) and Bayesian Inference (BI) in CIPRES (Miller et al. 2011).

BI analysis was based on the model adopted in PAUP* 4 and MrModeltest2 v2 (Nylander 2004). All sites in the loci were considered, and the analysis was performed for ten million generations, with the first 25% of the trees discarded and burned using the MrBayes v 3.7 tool available from CIPRES (https://www.phylo.org/). Posterior probability (PP) and tree topology were visualized using FigTree v 1.1.2 (Rambaut 2009). The consensus tree of the ML and BI analyses was generated manually from the topology obtained by FigTree in ML analysis with the bootstrap values, plus the posterior probability values generated by the BI analysis, using the CorelDraw editing package 2020.

For the clade level analysis of the isolates obtained in the study, a phylogenetic inference using the Maximum Likelihood (ML) method was performed with 1,000 replicates in the IQ-TREE platform (http://iqtree.cibiv.univie.ac.at/). This was based on the dataset of partial sequences of the RPB2 gene of representative species of all clades, as reported in the authoritative guidelines on molecular identification of Trichoderma (Cai and Druzhinina 2021).

Antagonistic activity

The inhibitory effect was estimated in vitro by using paired-cultures of T. juruarense against the plant pathogens Sclerotium rolfsii, Colletotrichum siamense, Fusarium decemcellulare and Corynespora cassiicola (Table 3). Trichoderma isolates were grown for 7 days in PDA and 8 mm plugs were used for the paired culture. The plant pathogens were pre-incubated for the antagonism assay according to the growing speed of each pathogen. The only pathogen without an incubation period was Sclerotium rolfsii, due to its fast-growing characteristics. For Colletotrichum siamense, a pre-incubation period of 2 days was adopted. For Fusarium decemcellulare and for Corynespora cassiicola, 5 days and 3 days were adopted, respectively. Plugs were placed on opposite sides of the plate containing the pre-incubated pathogen, with 5 cm between plugs and 1 cm from the plate’s edge. The culture was kept at 25 °C under a photoperiod of 12:12 h light-dark for 7 days. As a control, the plant pathogens were inoculated without the presence of a Trichoderma strain. The area of plant pathogen radial growth was determined using ImageJ (Schneider et al. 2012) and the inhibition of plant pathogens by Trichoderma was measured based on the relationship between control plates and paired culture using the following formula (Erazo et al. 2021):

Where, C: control area, and T: area of the pathogen under the influence of a Trichoderma isolate.

Phylogenetic analysis

The alignment used in the phylogenetic analyses for species delimitation resulted in 1,218 characters including gaps, in which the TEF contributed 551 characters and RPB2 667 characters. The best model adopted by PAUP*4 for TEF and RPB2 in the BI data was GTR+I+G. For the ML analysis, the best fitting model was TN+F+I+G4 for TEF and TIM3e+I+G4 for RPB2. All isolates of this study grouped together with high PP and bootstrap values and formed a sister clade with T. cyanodichotomus. This data, in conjunction with morphological analysis, supported the proposition of a new fungal species, named here as Trichoderma juruarense (Fig. 1).

The phylogram generated by the phylogenetic analysis of partial sequences of the RPB2 gene from representative species of all known Trichoderma clades indicated that all the isolates used in this study grouped with the invalidly named species Trichoderma cyanodichotomus, thus forming a distinct monophyletic clade, named here as clade 9 (Fig. 2).

Taxonomy

Trichoderma juruarense, R. Gwinner; T.F. Sousa and G.F. Silva, sp. nov., Fig. 1, Fig. 3; Mycobank: MB842019 accession numbers: ITS = OL639121; RPB2= OL782574; TEF = OL782580.

Etymology: refers to the Juruá River located in Brazilian Amazon

Holotype: INPA 0108

Macromorphology: Colonies at 25 °C and growing for 72 hours in PDA medium present white mycelium of a cottony appearance in the center and translucent sparse aerial mycelium at the border with low conidia and conidiophore production. No pigment or exudate production was observed. Colony radius after 72 h on PDA. Optimum growth temperature at 30 °C, 69.8–75 mm, 48.4–54.2 mm at 25 °C and 7.4–30.8 mm at 35 °C (Fig. 3). Colonies at 25 °C and growing for 7 days in CMA medium present white mycelium. Most colonies at 25 °C and growing for 7 days in CMA medium present white mycelium of a cottony appearance in the center and border, but can also present homogeneous white cottony mycelium. No pigment or exudate production was observed. Colony radius after 72 h on CMA. Optimum growth temperature at 30 °C 45.9–48.5 mm and 37.3–40.2 mm at 25 °C, absent at 35 °C (Fig. 3). Colonies at 25 °C and growing for 7 days in SNA medium present a homogeneous, translucent, sparse, aerial mycelium. No exudate or pigment production. Colony radius after 72 h on SNA. Optimum growth temperature at 30 °C 35.1–39.3 mm, 27.8–44.9 mm at 25 °C and 14.1–27 mm at 35 °C (Fig. 3).

Micromorphology: conidiophores present smooth-walls containing 2–3 lageniform phialides with a size of 4.33–6.48 μm (M = 5.01) 6.61–7.28 μm (M = 6.31 μm) and with the presence of green globose to obovoid macroconidia measuring 1.72–3.36 μm (M = 1.93 μm) 1.32–2.73 μm (M = 1.53 μm) and microconidia with a length of 0.96–1.54 (M = 1.2) 1.01–1.22 (M = 1.1) (Fig. 3). Presence of chlamydospores with 4.94–7.28 μm (M=6.99 μm) 6.61–7.28 μm (M = 6.31 μm) (Fig. 3).

Sexual stage: Not observed

Distribution: Brazil, Amazon.

Notes: Differs from T. cyanodichotomus by its smaller conidia and chlamydospores sizes, as well as low conidiophore production in 7 days growing at 25 °C in PDA media, and absence of abundant blue-green pigmentation under these conditions.

Antagonistic activity

T. juruarense presented in vitro inhibition for all tested phytopathogens (Table 3 and Fig. 4), and it also promoted mean inhibition values ranging from 43% to 61% against plant pathogens. The pattern of inhibition against distinct pathogens suggests that T. juruarense should be studied as a potential biocontrol agent. T. juruarense apparently inhibited the phytopathogens through competition, but further studies are still necessary in order to understand the metabolic response of T. juruarense during the inhibition process.

The Amazonian biome hosts a rich fungal biodiversity and, even with numerous reports of new fungi species from this biome, the number of novel species of Trichoderma isolated from the Brazilian Amazon is still low when compared to the great diversity of Amazonian species (Ritter et al. 2020). In this paper, a new Trichoderma species is described and a new clade is proposed. T. juruarense is closely related to two Trichoderma species: T. cyanodichotomus and T. lycogaloides. T. cyanodichotomus is currently under an invalid name due to lack of compliance with “The International Code of Nomenclature for algae, fungi, and plants” (Turland et al. 2018), therefore the identification of closely related species may contribute to a better understanding of Trichoderma taxonomy. Previously classified as a species of Sarawakus, S. lycogaloides was revised several times until it was categorized as a Trichoderma species under the name of T. lycogaloides (Jaklitsch et al. 2014). The phylogenetic relationship of T. juruarense with the most closely related species reveals a distinct clade of Trichoderma.

Phylogenetically, T. juruarense is closely related to T. cyanodichotomus with few SNP’s (single nucleotide polymorphisms) in the partial sequences of TEF and RPB2 genes in relation to T. cyanodichotomus, but isolates related in the present study collected in different points along the river, share the same SNP’s. These molecular data, in conjunction with morphological characters such as conidia and chlamydospores sizes, reinforce the proposition of T. juruarense sp. nov.

The taxonomy of the Trichoderma genera was recently revisited and a clade system based on RPB2 sequence data was proposed (Cai and Druzhinina 2021). Herein, we perform a phylogenetic inference using RPB2 sequences from representative species belonging to all known clades, including for the first time the species T. cyanodichotomus and T. juruarense sp. nov.. Surprisingly, both species formed a monophyletic clade and were not grouped with any other species. To provide continuity of this systematization of the clade, we denominate this distinct clade as clade 9. Our data indicate that T. lycogaloides formed a sister clade with clade 9 and separate from clade 1 (Fig. 1).

Similarly, to T. cyanodichotomus, the blue-green pigment was observed for T. juruarense sp. nov. Nonetheless, this feature seems inconstant and presents an uneven pattern under in vitro conditions, while T. cyanodichotomus presents a homogeneous production of blue-green pigment in CMA medium (Li et al. 2018).

Trichoderma juruarense sp. nov. showed in vitro inhibition of phytopathogens of agricultural importance and may be a promising ally in biological control, as has already been observed in other species of Trichoderma (Moutassem et al.; Ghazanfar et al. 2018; Díaz-Gutiérrez et al. 2021). In view of the biotechnological potential of this species, further studies of the whole genome and metabolomics that explore the secondary metabolite arsenal will be the next steps for this new fungal species.

Herein, we presented a novel species of Trichoderma that is closely related to an isolate currently under an invalid species name. Therefore, with the aim of a better taxonomic resolution of the genus Trichoderma, this work contributes to resolving this taxonomic issue via the first described species belonging to this group under a legitimate name. Furthermore, our data indicate that the monophyletic group composed by T. juruarense and T. cyanodichotomus is a new Trichoderma clade.

Author contributions

Gwinner R. concebeu e planejou os experimentos. Sousa, T.F foi responsável pela análise filogenética. Bandeira, I.C foi responsável pela análise morfológica. Sousa, S. B e Castro, G.S foram responsáveis pelos testes de antagonismo e Silva G.F é o líder da pesquisa e orientou o desenvolvimento do estudo, Koolen H.H, Hanada R.E, Faria, J.V supervisionaram os resultados deste trabalho. Todos os autores discutiram e corrigiram o texto e contribuíram para o manuscrito final. All the authors read and approved the final manuscript.

Funding

This work was funded by the National Council for Scientific and Technological Development (CNPq grant 435705/2018-0), National Council for the Improvement of Higher Education Personnel (CAPES- grant number 88881.200469/2018-01 Procad AmazonMicro and Grant Nº 88887.510218-2020-00 CAPES-Amazônia-Legal), FAPEAM (Amazonas State Research Support Foundation grants: Amazonas Estratégico 062.01311/2018 for G.F.S., 062.01303/2018 for H.H.F.K. and 01.02.016301.01750/2021 for JVF).

Acknowledgments

The authors would like to thank the Independent Center for Analysis of Biomedical Phenomena (CMABio) and the Amazonas State University (UEA) for their support in the activities of Electron Microscopy. The authors are also very grateful for the contribution of Jeferson Chagas da Cruz who collected sediments from the Juruá River that resulted in the isolation of the new species T. juruarense and for the exceptional technical support provided.

Conflict of interest: The authors declare no competing interests.

Legal authorizations:

Ministry of Environment - Council for the Management of Genetic Patrimony - (CGEN)

National Management System of the Genetic Patrimony and Associated Traditional Knowledge (SISGEN)

SISGEN Accession Registration: No AB6B14F

Date availability

Datasets generated and analyzed during the current study are available either in GenBank at NCBI (National Center for Biotechnology Information) or included in this published article (and its supplementary information files).

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Table 1 Comparison of morphological traits of Trichoderma juruarense and closely related species. *M = mean value.

	*T. juruarense* sp. nov.	*T. lycogaloides* (Jaklitsch et al. 2014)	*T. cyanodichotomus* (Li et al. 2018)
Macroconidia	obovoid, smooth, green or yellowish green	oval or subglobose, rarely oblong green, thick-walled, smooth, eguttulate	Macro: ellipsoidal to obovoid, smooth-walled, green or yellowish green
length (µm)	(1.72)1.93–2.70(3.36) (M = 2.31 μm)	(6.5)9.5–13.5(15.0)	3.7–5.5 μm
width (µm)	(1.32)1.53–2.19(2.73) (M=1.84 μm)	(5.8)8.0–11.5(12.5)	3.4–4.6 µm
L/W ratio	(1.01)1.13–1.38(1.68) (M=1.26)
Microconidia	green, globose	not observed	green, generally globose
length (µm)	0.96–1.54 µm (M= 1.2)	-	1.0–2.3 μm
width (µm)	1.01–1.22 µm (M=1.1)	-	1.0–2.2 µm
L/W ratio
Phialide	lageniform	cylindrical or lageniform	mostly lageniform and bowling pin shaped
length (µm)	(4.33)5.01–6.03(6.48) µm (M=5.45 µm)	22–43 µm	3.7–5.5 µm
width (µm)	(1.18)1.13–1.65(2.15) µm (M=1.47 µm)	4.2–7.5 µm	3.4–4.6 µm
L/W ratio	(2.96)3.4 –4.05(4.02) µm (M=3.76 µm)	3.5–7.6 µm	-
Chlamydospore	subglobose	not observed	subglobose to ellipsoidal, easily deciduous, massively produced on PDA
length (µm)	4.94–7.28 µm (M=6.99 μm)	-	7.3–12.6 μm
width (µm)	6.61–7.28 µm (M = 6.31 μm)	-	5.3–9.7 µm
L/W ratio	0.78–1.53 µm	-	-

Table 2 - Taxa used in the phylogenetic analysis, strain and GenBank accession numbers.

			Genbank accession numbers			Reference
Species	Strain	Clade	ITS	RPB2	TEF
*T. juruarense* sp. nov.	INPA 0108^T	Clade 9	OL639121	OL782574	OL782580	In this study
*T. juruarense* sp. nov.	INPA 0105	Clade 9	OL639119	OL782576	OL782581	In this study
*T. juruarense* sp. nov.	INPA 0106	Clade 9	OL639120	OL782577	OL782579	In this study
*T. juruarense* sp. nov.	INPA 0111	Clade 9	OL639122	OL782578	OL782582	In this study
*T. juruarense* sp. nov.	INPA 0149	Clade 9	OL639123	OL782575	OL782583	In this study
Arachnocrea scabrida	BEO 02-01	-	-	DQ834458.1	DQ834457.1	(Overton et al. 2006)
Arachnocrea stipata	-	-	-	EU710770.1	-	(Jaklitsch et al. 2008b)
T. lycogaloides	SL^T	Clade 1	-	KF134792.1	KF134800.1	(Jaklitsch et al. 2014)
T. tibetense	HMAS 245010^T	Clade 1	NR_144881.1	KT735261.1	KT735254.1	(Chen and Zhuang 2016)
T. chlamydosporicum	HMAS 248850^T	Clade 1	NR_154577.1	KY687989.1	KY688052.1	(Chen and Zhuang 2017a)
T. strictipile	CBS 347.93^T	Clade 1	NR_134337.1	KJ842182.1	AY865644.1	(Druzhinina et al. 2005)
T. tropicosinense	HMAS 252546^T	Clade 1	NR_134441.1	KF923313.1	KF923286.1	(Zhu and Zhuang 2015a)
T. longipile	CBS 120953^T	Clade 1	NR_134354.1	FJ860542.2	FJ860643.1	(Jaklitsch 2009)
T. shennongjianum	HMAS 245009^T	Clade 1	NR_144880.1	KT735259.1	KT735253.1	(Chen and Zhuang 2016)
T. phyllostachydis	GJS 92-123^T	Clade 1	AY737755.1	AF545513.1	AY737745.1	(Chaverri et al. 2003)
T. ganodermatis	HMAS 248856^T	Clade 1	NR_154581.1	KY687995.1	KY688060.1	(Chen and Zhuang 2017a)
T. crassum	GJS 01-227	Clade 1	MH862406.1	AY481587.1	JN133572.1	(Chaverri and Samuels 2013)
T. chromospermum	GJS 94-67	Clade 1	AY737774.1	AY391912.1	AY737728.1	(Chaverri and Samuels 2003)
T. gliocladium	CBS 130009^T	Clade 1	NR_160252.1	KJ665271.1	KJ665502.1	(Jaklitsch and Voglmayr 2015)
T. hainanense	HMAS 248837^T	Clade 1	NR_154568.1	KY687976.1	KY688033.1	(Chen and Zhuang 2017a)
T. silvae-virgineae	CBS 120922^T	Clade 1	NR_134414.1	FJ860587.1	FJ860696.1	(Jaklitsch 2011)
T. helicum	DAOM 230016	Clade 1	DQ083022.1	KJ842200.1	EU280055.1	(Bissett et al. 2015)
T. byssinum	HMAS 248839	Clade 1	KY687922.1	KY687978.1	KY688036.1	(Chen and Zhuang 2017a)
T. hebeiense	HMAS 248743^T	Clade 1	NR_153278.1	KX344439.1	KX344434.1	(Chen and Zhuang 2017b)
T. sichuanense	HMAS 248736	Clade 1	KY014087.1	KX344436.1	KX344427.1	(Chen and Zhuang 2017b)
T. verticillatum	HMAS 248740^T	Clade 1	KY014091.1	KX344438.1	KX344431.1	(Chen and Zhuang 2017b)
T. rossicum	DAOM 230011^T	Clade 1	HQ342419.1	KJ842191.1	AY937441.1	(Samuels 2006)
T. barbatum	GJS 04-308^T	Clade 1	NR_134430.1	HQ342286.1	HQ342223.1	(Samuels et al. 2012)
T. floccosum	GJS 01-238^T	Clade 1	NR_137306.1	HQ342281.1	HQ342218.1	(Robbertse et al. 2017)
T. ivoriense	GJS 01-312^T	Clade 1	HQ342411.1	HQ342280.1	HQ342217.1	(Bissett et al. 2015)
T. stromaticum	GJS 97-183^T	Clade 1	AF097913.1	HQ342245.1	AY937418.1	(Samuels et al. 2000)
T. vermipilum	PPRI 3559^T	Clade 1	AF400268.1	HQ342282.1	HQ342219.1	(Kullnig-Gradinger et al. 2002)
T. caesareum	GJS 01-225^T	Clade 1	NR_134427.1	HQ342279.1	HQ342216.1	(Robbertse et al. 2017)
T. medusae	GJS 01-171^T	Clade 1	NR_134426.1	HQ342277.1	HQ342214.1	(Robbertse et al. 2017)
T. lanuginosum	GJS 01-176^T	Clade 1	NR_134429.1	HQ342284.1	HQ342221.1	(Robbertse et al. 2017)
T. spirale	DAOM 183974^T	Clade 1	NR_077177.1	AF545553.1	EU280049.1	(Robbertse et al. 2017)
T. pyramidale	CBS 135574^T	Clade 1	KX632513.1	KJ665334.1	KJ665699.1	(Jaklitsch and Voglmayr 2015)
T. afroharzianum	GJS 04-02	Clade 1	NR_137304.1	FJ442691.1	FJ463401.1	(Bissett et al. 2015)
T. harzianum	CBS 227.95	Clade 1	AF057605.1	AF545549.1	AF348100.1	(Samuels et al. 2002)
T. inhamatum	CBS 273.78^T	Clade 1	NR_134378.1	FJ442725.1	AF348099.1	(Robbertse et al. 2017)
T. afarasin	CBS 130755^T	Clade 1	NR_137301.1	FJ442799.1	AF348093.1	(Chaverri et al. 2015)
T. cyanodichotomus	TW21990-1^T	Clade 1	KY189312.1	KY707175.1	KY707174.1	(Li et al. 2018)
T. fassatiae	CCF 5000	Clade 2	LN866275.1	LN866276.1	LN866277.1	(Nováková et al. 2015)
T. fertile	DAOM 167161^T	Clade 2	NR_134336.1	AF545546.1	KJ871131.1	(Chaverri et al. 2003)
T. fomiticola	CBS 121136^T	Clade 2	NR_134391.1	FJ860538.1	FJ860639.1	(Jaklitsch 2009)
T. hunua	CBS 238.63^T	Clade 2	NR_160091.1	KJ665279.1	KJ665519.1	(Jaklitsch and Voglmayr 2015)
T. mienum	TUFC 61533^T	Clade 2	NR_134433.1	AB856754.1	JQ621978.1	(Kim et al. 2012)
T. moravicum	CBS 120539^T	Clade 2	NR_134398.1	FJ860548.1	FJ860651.1	(Jaklitsch 2011)
T. oblongisporum	DAOM 176226^T	Clade 2	NR_138437.1	KJ842199.1	KJ871142.1	(Bissett et al. 2015)
T. semiorbis	GJS 99-108^T	Clade 2	NR_134423.1	JN133567.1	JN133576.1	(Chaverri and Samuels 2013)
T. euskadiense	CBS 130013^T	Clade 3	NR_160254.1	KJ665269.1	KJ665492.1	(Jaklitsch and Voglmayr 2015)
T. sinense	DAOM 230004^T	Clade 3	NR_134425.1	JN175528.1	AY750889.1	(Druzhinina et al. 2012)
T. konilangbra	GJS 96-147^T	Clade 3	MH862712.1	KJ665284.1	AY937425.1	(Samuels 2006)
T. flagellatum	PPRC-ET58	Clade 3	MH865822.1	JN258688	FJ763184.1	(Druzhinina et al. 2012)
T. parareesei	TUB F-1066^T	Clade 3	MH863773.1	HM182963.1	GQ354353.1	(Atanasova et al. 2010)
T. reesei	CBS 383.78^T	Clade 3	Z31016	HM182969.1	DQ025754.2	(Atanasova et al. 2010)
T. orientale	GJS 04-321	Clade 3	NR_111317.1	JN175522.1	JN175573.1	(Druzhinina et al. 2012)
T. bissettii	CBS 137447^T	Clade 3	NR_134442.1	KJ665244.1	HG931266.1	(Sandoval-Denis et al. 2014)
T. longibrachiatum	CBS 816.68^T	Clade 3	EU401556.1	DQ087242.1	AY865640.1	(Druzhinina et al. 2005)
T. alcalifuscescens	TFC 00-36^T	Clade 4	FJ860722.1	DQ834462.1	FJ860610.1	(Overton et al. 2006)
T. delicatulum	CBS 120631^T	Clade 4	FJ860751.1	FJ860535.1	FJ860636.1	(Jaklitsch 2011)
T. parmastoi	TFC 97-143^T	Clade 4	NR_134405.1	DQ834463.1	FJ860669.1	(Jaklitsch and Voglmayr 2013)
T. peltatum	GJS 08-207^T	Clade 4	NR_134422.1	HQ260610.1	KR135819.1	(Samuels and Ismaiel 2011)
T. polyalthiae	UBZSN2-1^T	Clade 4	MF135132.1	LC373011.1	LC328976.1	(Nuankaew et al. 2018)
T. asperelloides	GJS 04-116	Clade 5	GU198301.1	GU248411.1	GU248412.1	(Samuels et al. 2010)
T. asperellum	CBS 433.97^T	Clade 5	NR_130668.1	EU248617	AY376058.1	(Bissett et al. 2015)
T. atroviride	CBS 142.95^T	Clade 5	AY380906.1	EU341801.1	AF456891.1	(Bissett et al. 2015)
T. gamsii	GJS 04-09	Clade 5	DQ315459.1	JN133561.1	DQ307541.1	(Samuels et al. 2006a)
T. hamatum	DAOM 167057^T	Clade 5	NR_134371.1	AF545548.1	AF456911.1	(Bissett et al. 2015)
T. koningii	CBS 457.96^T	Clade 5	MH862585.1	FJ442761	KC285594.1	(Jaklitsch et al. 2013)
T. ovalisporum	Dis70a^T	Clade 5	AY380897.1	FJ442742.1	AY376037.1	(Holmes et al. 2004)
T. stilbohypoxyli	CBS 992.97^T	Clade 5	DQ313152.1	EU341805	DQ109546.1	(Samuels et al. 2006a)
T. strigosellum	CPK 3604^T	Clade 5	NR_134437.1	EU248607.1	JQ425705.1	(López-Quintero et al. 2013)
T. strigosum	CBS 348.93^T	Clade 5	NR_103571.1	AF545556	AY376057.1	(López-Quintero et al. 2013)
T. theobromicola	Dis 85f ^T	Clade 5	NR_134359.1	FJ007374	EU856321.1	(Samuels et al. 2006b)
T. viride	CBS 119325^T	Clade 5	NR_138441.1	EU711362.2	DQ672615.2	(Jaklitsch et al. 2008b)
T. arundinaceum	GJS 05-180	Clade 6	EU330928.1	EU338303.1	EU338275.1	(Degenkolb et al. 2008)
T. aurantioeffusum	CBS 119284^T	Clade 6	NR_134383.1	FJ860520.1	FJ860613.1	(Jaklitsch 2011)
T. brevicompactum	GJS 04-381	Clade 6	EU330941.1	EU338317.1	EU338299.1	(Degenkolb et al. 2008)
T. deliquescens	CBS 121132	Clade 6	NR_134394.1	FJ179609.1	FJ860644.1	(Jaklitsch et al. 2008a)
T. luteocrystallinum	CBS 123828^T	Clade 6	NR_134396.1	FJ860544.1	FJ860646.1	(Jaklitsch 2011)
T. margaretense	C.P.K. 3127^T	Clade 6	FJ860741.1	FJ860529.1	FJ860625.1	(Jaklitsch 2011)
T. melanomagnum	GJS 99-153^T	Clade 6	AY737770.1	AY391926.1	AY737751.1	(Chaverri and Samuels 2003)
T. protrudens	DIS 119F^T	Clade 6	NR_134373.1	EU338322.1	EU338289.1	(Degenkolb et al. 2008)
T. rodmanii	GJS 91-88^T	Clade 6	NR_134374.1	EU338324.1	EU338286.1	(Degenkolb et al. 2008)
T. turrialbense	CBS 112445^T	Clade 6	NR_138448.1	EU338321.1	EU338284.1	(Degenkolb et al. 2008)
T. applanatum	HMAS 266666^T	Clade 7	NR_134443.1	KJ634726.1	KJ634759.1	(Zhu and Zhuang 2015b)
T. austriacum	CBS 122494^T	Clade 7	NR_134384.1	FJ860525.1	FJ860619.1	(Jaklitsch 2011)
T. calamagrostidis	CBS 121133^T	Clade 7	NR_134386.1	FJ860528.1	FJ860622.1	(Jaklitsch 2011)
T. ceciliae	CBS 130010^T	Clade 7	NR_160253.1	KJ665247.1	KJ665444.1	(Jaklitsch and Voglmayr 2015)
T. citrinum	C.P.K. 960	Clade 7	NR_134368.1	AF545561.1	FJ860631.1	(Bissett et al. 2015)
T. decipiens	CBS 121307^T	Clade 7	EF558546.1	KJ665256.1	FJ860635.1	(Jaklitsch and Voglmayr 2015)

Ex-type strains are indicated in ^“T” after the collection number

Table 3 Percentage of growth inhibition of plant pathogens by Trichoderma juruarense.

Pathogen	ID	Collection	Inhibition (%)	SD (%)
Sclerotium rolfsii	2941	INPA	51	31
Colletotrichum siamense	Coll 2N	Embrapa CPAA	50	2.5
Fusarium decemcellulare	307	Embrapa CPAA	61	14
Corynespora cassiicola	2671	INPA	43	11

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posted 10 Jan, 2022

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Trichoderma juruarense sp. nov. (Hypocreaceae) a new fungal species from sediments of the Amazonian Juruá River with agricultural potential

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