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Mycological Progress

, Volume 18, Issue 9, pp 1135–1154 | Cite as

New plectosphaerellaceous species from Dutch garden soil

  • Alejandra GiraldoEmail author
  • Margarita Hernández-Restrepo
  • Pedro W. Crous
Open Access
Original Article
  • 502 Downloads

Abstract

During 2017, the Westerdijk Fungal Biodiversity Institute (WI) and the Utrecht University Museum launched a Citizen Science project. Dutch school children collected soil samples from gardens at different localities in the Netherlands, and submitted them to the WI where they were analysed in order to find new fungal species. Around 3000 fungal isolates, including filamentous fungi and yeasts, were cultured, preserved and submitted for DNA sequencing. Through analysis of the ITS and LSU sequences from the obtained isolates, several plectosphaerellaceous fungi were identified for further study. Based on morphological characters and the combined analysis of the ITS and TEF1-α sequences, some isolates were found to represent new species in the genera Phialoparvum, i.e. Ph. maaspleinense and Ph. rietveltiae, and Plectosphaerella, i.e. Pl. hanneae and Pl. verschoorii, which are described and illustrated here.

Keywords

Biodiversity Citizen Science project Phialoparvum Plectosphaerella Soil-born fungi 

Introduction

Soil is one of the main reservoirs of fungal species and commonly ranks as the most abundant source regarding fungal biomass and physiological activity. Fungal diversity is affected by the variety of microscopic habitats and microenvironments present in soils (Anderson and Domsch 1978; Bills et al. 2004). More than half of the soil mycobiota is composed of basidiomycetes, although they are overlooked by most isolation techniques (Kirk et al. 2001). The remaining fungal biomass is comprised by Ascomycota, Chytridiomycota, Mucorales and Oomycetes (Kirk et al. 2001; Bills et al. 2004; Crous et al. 2019). This observed species richness has been supported by the discovery of previously unrecognised phylogenetic fungal lineages in soil-inhabiting fungi (Tedersoo et al. 2017).

Among Ascomycota, the family Plectosphaerellaceae (Glomerellales, Sordariomycetes) harbours important plant pathogens such as Verticillium dahliae, V. alboatrum and Plectosphaerella cucumerina, but also several saprobic genera usually found in soil, i.e. Chordomyces, Gibellulopsis and Sodiomyces (Domsch et al. 2007; Zare et al. 2007; Carlucci et al. 2012; Grum-Grzhimaylo et al. 2013, 2016). Members of this family are mainly known from their asexual morphs, which are morphologically characterised by simple or verticillate conidiophores with mono- or polyphialidic conidiogenous cells, and 1- or 2-celled elongate conidia arranged in slimy heads or chains, and rarely produced sporodochia or synnemata. The sexual morph is mostly observed in culture, showing perithecial or cleistothecial ascomata, superficial, brown to dark brown, with clavate or saccate asci and hyaline to pale brown ascospores (Giraldo and Crous 2019).

The interest in soil fungi has recently increased due to the high demand for new compounds with application in the biotechnological or pharmaceutical industries (Hujslová et al. 2010), and also because this substratum contains a pool of interesting and undescribed species, especially when samples from diverse habitats are studied (Blackwell 2011; Tedersoo et al. 2014, 2017). Therefore, during 2017, children from different locations in the Netherlands collected soil samples which were analysed in order to find new fungal species. This was done during the course of a Citizen Science project, named ‘Wereldfaam, een schimmel met je eigen naam’ (World fame - a fungus with your name) coordinated by the Westerdijk Fungal Biodiversity Institute and the Utrecht University Museum. Among the examined samples, several plectosphaerellaceous fungi were isolated, some of which have been recently described as new species in the genera Gibellulopsis and Lectera (Crous et al. 2018), while others represent new species in the genera Phialoparvum and Plectosphaerella, which are described and illustrated here.

Materials and methods

Sampling and isolation

Protocols for the collection and processing of soil samples are described in Groenewald et al. (2018). After 1 week of incubation on MEA supplemented with penicillin-G and streptomycin, individual colonies were transferred to MEA plates without antibiotics and incubated between 22 and 24 °C for 7–14 days, in order to obtain axenic cultures. Subsequently, each isolate was submitted for DNA extraction and sequencing. All isolates are maintained in the Johanna Westerdijk (JW) collection housed at the Westerdijk Fungal Biodiversity Institute in Utrecht, The Netherlands. Isolates from new and interesting species are also deposited at the CBS Culture Collection at the WI.

DNA extraction, amplification and sequencing

Total genomic DNA was extracted from colonies growing on MEA using the Wizard® Genomic DNA Purification Kit (Promega Corporation, Madison, WI, USA), following the manufacturer’s protocol. The internal transcribed spacer (ITS) regions and the 5′ end of the 28S nrDNA gene (LSU) were amplified for all isolates with the primer combination ITS5/LR5, and sequenced with the primer pairs ITS5/ITS4 (White et al. 1990) and LR0R/LR5 (Vilgalys and Hester 1990; Vilgalys and Sun 1994), respectively. Additional loci were sequenced for some isolates, including fragments from the protein-coding genes translation elongation factor 1-alpha (TEF1-α) and RNA polymerase II second largest subunit (RPB2) with the primer sets EF-983F/EF-2218R (Rehner and Buckley 2005) and RPB2-5F2/RPB2-7cR (Liu et al. 1999), respectively. The consensus sequence of each locus was obtained by using the program SeqMan v. 12.1.0 (DNASTAR, Madison, WI, USA).

Species identification

Firstly, the LSU and ITS consensus sequences from each isolate were blasted against sequences available in NCBI (http://blast.ncbi.nlm.nih.gov) and CBS (http://www.westerdijkinstitute.nl/Collections) databases, in order to determine the generic placement of each isolate. Secondly, sequences from all isolates identified as members of the Plectosphaerellaceae were aligned with sequences from ex-type and reference strains of the species currently accepted in the genera (Table 1) to which each isolate belonged. Separate analyses based on ITS or ITS combined with TEF1-α were performed for those isolates that were not identified at level species by using the previous approach.
Table 1

Details of the isolates used in this study. New generated sequences are in bold

Species

Isolate nr.

Source

Locality

GenBank/ENA accession no.

   

Reference

LSU

ITS

TEF1-α

RPB2

Acrostalagmus luteoalbus

CBS 121214

Musa sapientum

Brazil, Minas Gerais, Viçosa

LR025791

LR026662

Giraldo and Crous (2019)

 

JW 1001

Garden soil

The Netherlands, Amsterdam

LR590267

LR590089

This study

 

JW 1049

Garden soil

The Netherlands, Amsterdam

LR590269

LR590090

This study

 

JW 10014

Garden soil

The Netherlands, Utrecht

LR590268

This study

 

JW 22005

Garden soil

The Netherlands, Vlissingen

LR590271

LR590092

This study

 

JW 22008

Garden soil

The Netherlands, Vlissingen

LR590272

LR590093

This study

 

JW 22010

Garden soil

The Netherlands, Vlissingen

LR590273

LR590094

This study

 

JW 22029

Garden soil

The Netherlands, Vlissingen

LR590274

LR590095

This study

 

JW 57005

Garden soil

The Netherlands, Capelle aan den Ijssel

LR590098

This study

 

JW 59014

Garden soil

The Netherlands, Utrecht

LR590099

This study

 

JW 145012

Garden soil

The Netherlands, Wageningen

LR590270

LR590091

This study

 

JW 234011

Garden soil

The Netherlands, Born

LR590275

LR590096

This study

 

JW 234012B

Garden soil

The Netherlands, Born

LR590097

This study

 

JW 263015

Garden soil

The Netherlands, Utrecht

LR590276

This study

A. annulatus

DAOMC 212126

Soil and roots

Brazil, Pará, near Belen

GU180646

GU180632

Réblová et al. (2011)

Brunneochlamydosporium cibotii

CBS 109240IT

Cibotium schiedei

The Netherlands, Delft

LR025807

LR026678

Giraldo and Crous (2019)

B. macroclavatum

CBS 101249T

Pteridophyte

Mauritius

LR025811

LR026682

Giraldo and Crous (2019)

 

JW 10015 = CBS 145320

Garden soil

The Netherlands, Utrecht

LR590277

LR590100

LR594766

LR594787

This study

B. nepalense

CBS 971.72T

Soil under Pinus sp.

Nepal, Himalaya septentrional

LR025813

LR026684

Giraldo and Crous (2019)

 

CBS 277.89

Soil

Unknown

LR025812

LR026683

Giraldo and Crous (2019)

 

CBS 113254

Scrub sandy soil

The Netherlands, Kwade Hoek

LR025815

LR026686

Giraldo and Crous (2019)

 

CBS 116720

Scrub sandy soil

The Netherlands, Kwade Hoek

LR025816

LR026687

Giraldo and Crous (2019)

 

CBS 116721

Scrub sandy soil

The Netherlands, Kwade Hoek

LR025817

LR026688

Giraldo and Crous (2019)

 

CBS 116722

Scrub sandy soil

The Netherlands

LR025818

LR026689

Giraldo and Crous (2019)

 

JW 5014

Garden soil

The Netherlands, Nieuwegein

LR590285

This study

 

JW 13002

Garden soil

The Netherlands, Alkmaar

LR590278

LR590101

This study

 

JW 17010

Garden soil

The Netherlands, Ravenswaaij

LR590281

LR590104

This study

 

JW 17016

Garden soil

The Netherlands, Ravenswaaij

LR590282

LR590105

This study

 

JW 17026

Garden soil

The Netherlands, Ravenswaaij

LR590283

LR590106

This study

 

JW 141012

Garden soil

The Netherlands, Kortenhoef

LR590279

LR590102

This study

 

JW 147024

Garden soil

The Netherlands, Utrecht

LR590280

LR590103

This study

 

JW 263017

Garden soil

The Netherlands, Utrecht

LR590284

LR590107

This study

Chordomyces albus

CBS 987.87T

Hypogymnia physodes

Luxembourg

JX158444

DQ825970

Grum-Grzhimaylo et al. (2013), Zare et al. (2007)

 

JW 1007

Garden soil

The Netherlands, Amsterdam

LR590286

LR590108

This study

 

JW 16023

Garden soil

The Netherlands, Reeuwijk

LR590290

LR590113

This study

 

JW 25004

Garden soil

The Netherlands, Hooglanderveen

LR590300

LR590123

This study

 

JW 96001

Garden soil

The Netherlands, Leiden

LR590301

LR590124

This study

 

JW 143002

Garden soil

The Netherlands, Utrecht

LR590287

LR590109

This study

 

JW 144015

Garden soil

The Netherlands, Herten

LR590288

LR590110

This study

 

JW 149016

Garden soil

The Netherlands, Utrecht

LR590111

This study

 

JW 160002

Garden soil

The Netherlands, Houten

LR590289

LR590112

This study

 

JW 187003

Garden soil

The Netherlands, Soest

LR590291

LR590114

This study

 

JW 189008

Garden soil

The Netherlands, Weert

LR590292

LR590115

This study

 

JW 200003

Garden soil

The Netherlands, Houten

LR590293

LR590116

This study

 

JW 211012

Garden soil

The Netherlands, Utrecht

LR590294

LR590117

This study

 

JW 211015

Garden soil

The Netherlands, Utrecht

LR590295

LR590118

This study

 

JW 232015

Garden soil

The Netherlands, Nederweert

LR590296

LR590119

This study

 

JW 232019

Garden soil

The Netherlands, Nederweert

LR590297

LR590120

This study

 

JW 234007

Garden soil

The Netherlands, Born

LR590298

LR590121

This study

 

JW 234017

Garden soil

The Netherlands, Born

LR590299

LR590122

This study

C. antarcticus

CBS 120045T

Soda soil

Russia, Kulunda Steppe, Altai

KJ443109

KJ443241

Grum-Grzhimaylo et al. (2016)

 

JW 20003

Garden soil

The Netherlands, ‘s-Gravenhage

LR590304

LR590127

This study

 

JW 95011

Garden soil

The Netherlands, Warmond

LR590305

LR590128

This study

 

JW 96013

Garden soil

The Netherlands, Leiden

LR590306

LR590129

This study

 

JW 125029

Garden soil

The Netherlands, Amersfoort

LR590302

LR590125

This study

 

JW 150004

Garden soil

The Netherlands, Liempde

LR590303

LR590126

This study

Furcasterigmium furcatum

CBS 122.42T

Dune sand under Calystegia soldanella

France, Normandie, Pointe du Siège

LR025838

LR026709

Giraldo and Crous (2019)

 

JW 12002

Garden soil

The Netherlands, Breda

LR590307

LR590130

This study

 

JW 96018

Garden soil

The Netherlands, Leiden

LR590133

This study

 

JW 125004

Garden soil

The Netherlands, Amersfoort

LR590308

LR590131

This study

 

JW 170003

Garden soil

The Netherlands, Utrecht

LR590309

LR590132

This study

Fuscohypha expansa

CBS 103.95

Soil

Brazil

LR025844

LR026714

LR026411

Giraldo and Crous (2019)

 

CBS 418.89T

Tuber of Dioscorea sp.

Martinique

LR025845

LR026715

LR026412

Giraldo and Crous (2019)

Gibellulopsis aquatica

CBS 117131T

Cloud water

France

LR025850

LR026720

Giraldo and Crous (2019)

G. catenata

CBS 113951T

Cervical swab of mare

Germany

LR025851

LR026721

Giraldo and Crous (2019)

G. fusca

CBS 308.38

Apium graveolens

Germany, Giessen

LR025852

LR026722

Giraldo and Crous (2019)

 

CBS 402.80

Aegopodium podagraria

The Netherlands, Baarn

LR025853

LR026723

Giraldo and Crous (2019)

 

CBS 560.65T

Soil

India, Banaras

LR025854

LR026724

Giraldo and Crous (2019)

 

CBS 747.83

Apium graveolens

The Netherlands

LR025855

LR026725

Giraldo and Crous (2019)

 

JW 40010

Garden soil

The Netherlands, Goes

LR590633

This study

 

JW 40011

Garden soil

The Netherlands, Goes

LR590312

LR590135

This study

 

JW 122019

Garden soil

The Netherlands, Leiden

LR590310

LR590253

This study

 

JW 214001

Garden soil

The Netherlands, Nijkerk

LR590311

LR590134

This study

G. nigrescens

CBS 179.40

Wrapping material

The Netherlands, Rotterdam

LR025857

LR026727

Giraldo and Crous (2019)

 

CBS 455.51

Solanum tuberosum

United Kingdom

LR025858

LR026728

Giraldo and Crous (2019)

 

CBS 469.64

Seedling of Linum usitatissimum

Denmark, Klippinge

LR025859

LR026729

Giraldo and Crous (2019)

 

CBS 470.64

Medicago sativa

France

LR025860

LR026730

Giraldo and Crous (2019)

 

CBS 100833

Soil

Israel, Lahav

LR025864

LR026734

Giraldo and Crous (2019)

 

CBS 100844

Solanum tuberosum

Israel, Kerem-Shalom

LR025865

LR026735

Giraldo and Crous (2019)

 

CBS 100829

Solanum tuberosum

Israel, Kerem-Shalom

LR025862

LR026732

Giraldo and Crous (2019)

 

CBS 100832

Soil

Israel, Lahav

LR025863

LR026733

Giraldo and Crous (2019)

 

CBS 110719

Sandy soil

The Netherlands, Kwade Hoek

LR025866

LR026736

Giraldo and Crous (2019)

 

CBS 119666

Nail

The Netherlands

LR025867

LR026737

Giraldo and Crous (2019)

 

CBS 120949NT

Soil under lawn

The Netherlands, Baarn

LR025868

LR026738

Giraldo and Crous (2019)

 

CBS 123176

Moisture damaged building insulator wool

Finland

LR025869

LR026739

Giraldo and Crous (2019)

 

JW 4001

Garden soil

The Netherlands, Breda

LR590352

LR590175

This study

 

JW 4003

Garden soil

The Netherlands, Breda

LR590353

LR590176

This study

 

JW 18031

Garden soil

The Netherlands, Valkenswaard

LR590323

LR590146

This study

 

JW 22012

Garden soil

The Netherlands, Vlissingen

LR590330

LR590153

This study

 

JW 24012

Garden soil

The Netherlands, Utrecht

LR590341

LR590164

This study

 

JW 26002

Garden soil

The Netherlands, Soest

LR590343

LR590166

This study

 

JW 26005

Garden soil

The Netherlands, Soest

LR590344

LR590167

This study

 

JW 26011

Garden soil

The Netherlands, Soest

LR590345

LR590168

This study

 

JW 26030

Garden soil

The Netherlands, Soest

LR590346

LR590169

This study

 

JW 27001

Garden soil

The Netherlands, Vleuten

LR590349

LR590172

This study

 

JW 27033

Garden soil

The Netherlands, Vleuten

LR590350

LR590173

This study

 

JW 29026

Garden soil

The Netherlands, Oude Wetering

LR590351

LR590174

This study

 

JW 48001

Garden soil

The Netherlands, De Bilt

LR590354

LR590177

This study

 

JW 52010

Garden soil

The Netherlands, Driebergen-Rijsenburg

LR590355

LR590178

This study

 

JW 67017

Garden soil

The Netherlands, Zandvoort

LR590356

LR590179

This study

 

JW 79018

Garden soil

The Netherlands, Kapel Avezaath

LR590357

LR590180

This study

 

JW 80012

Garden soil

The Netherlands, Gouda

LR590358

LR590181

This study

 

JW 80013

Garden soil

The Netherlands, Gouda

LR590359

LR590182

This study

 

JW 85004

Garden soil

The Netherlands, Eibergen

LR590360

LR590183

This study

 

JW 96006

Garden soil

The Netherlands, Leiden

LR590361

LR590184

This study

 

JW 96011

Garden soil

The Netherlands, Leiden

LR590362

LR590185

This study

 

JW 126006

Garden soil

The Netherlands, Bunschoten-Spakenburg

LR590313

LR590136

This study

 

JW 130017

Garden soil

The Netherlands, Utrecht

LR590314

LR590137

This study

 

JW 132013

Garden soil

The Netherlands, Meteren

LR590315

LR590138

This study

 

JW 143007

Garden soil

The Netherlands, Utrecht

LR590316

LR590139

This study

 

JW 143017

Garden soil

The Netherlands, Utrecht

LR590317

LR590140

This study

 

JW 158004

Garden soil

The Netherlands, Houten

LR590318

LR590141

This study

 

JW 163008

Garden soil

The Netherlands, Amersfoort

LR590319

LR590142

This study

 

JW 169002

Garden soil

The Netherlands, Utrecht

LR590320

LR590143

This study

 

JW 171009

Garden soil

The Netherlands, Baarn

LR590321

LR590144

This study

 

JW 176011

Garden soil

The Netherlands, Utrecht

LR590322

LR590145

This study

 

JW 185004

Garden soil

The Netherlands, Ophemert

LR590324

LR590147

This study

 

JW 189031

Garden soil

The Netherlands, Weert

LR590325

LR590148

This study

 

JW 191001

Garden soil

The Netherlands, Amersfoort

LR590326

LR590149

This study

 

JW 191003

Garden soil

The Netherlands, Amersfoort

LR590327

LR590150

This study

 

JW 210002

Garden soil

The Netherlands, Heerenveen

LR590328

LR590151

This study

 

JW 214006

Garden soil

The Netherlands, Nijkerk

LR590329

LR590152

This study

 

JW 221006

Garden soil

The Netherlands, Houten

LR590331

LR590154

This study

 

JW 221021

Garden soil

The Netherlands, Houten

LR590332

LR590155

This study

 

JW 221027

Garden soil

The Netherlands, Houten

LR590333

LR590156

This study

 

JW 221030

Garden soil

The Netherlands, Houten

LR590334

LR590157

This study

 

JW 234005

Garden soil

The Netherlands, Born

LR590335

LR590158

This study

 

JW 234009

Garden soil

The Netherlands, Born

LR590336

LR590159

This study

 

JW 234014

Garden soil

The Netherlands, Born

LR590337

LR590160

This study

 

JW 234016

Garden soil

The Netherlands, Born

LR590338

LR590161

This study

 

JW 234022

Garden soil

The Netherlands, Born

LR590339

LR590162

This study

 

JW 236004

Garden soil

The Netherlands, Maasbracht

LR590340

LR590163

This study

 

JW 244014

Garden soil

The Netherlands, Jorwert

LR590342

LR590165

This study

 

JW 261004

Garden soil

The Netherlands, Utrecht

LR590347

LR590170

This study

 

JW 269002

Garden soil

The Netherlands, Utrecht

LR590348

LR590171

This study

G. serrae

CBS 125.79

Soil

New Zealand, Havelock North

LR025870

LR026740

Giraldo and Crous (2019)

 

CBS 175.75

Solanum tuberosum

Germany

LR025871

LR026741

Giraldo and Crous (2019)

 

CBS 290.30T

Human eye

Italy

LR025872

LR026742

Giraldo and Crous (2019)

 

CBS 345.39

Wood pulp

Sweden

LR025873

LR026743

Giraldo and Crous (2019)

 

CBS 383.66

Beta vulgaris var. altissima

Canada, Quebec

LR025874

LR026744

Giraldo and Crous (2019)

 

CBS 387.35

Amaranthus tricolour

Italy

LR025875

LR026745

Giraldo and Crous (2019)

 

CBS 392.89

Seed of Abelmoschus esculentus

Cuba, Santiago de las Vegas

LR025876

LR026746

Giraldo and Crous (2019)

 

CBS 493.82A

Soil of Glycine max

Argentina, Misiones, Cerro Azul

LR025878

LR026748

Giraldo and Crous (2019)

 

CBS 493.82B

Seed

Argentina, Buenos Aires, Castelar

LR025879

LR026749

Giraldo and Crous (2019)

 

CBS 493.82C

Seed

Argentina, Chaco, Las Brenas

LR025880

LR026750

Giraldo and Crous (2019)

 

CBS 493.82D

Seed

Argentina, Buenos Aires, Castelar

LR025881

LR026751

Giraldo and Crous (2019)

 

CBS 565.78A

Oidium sp.

Russia, Odessa

LR025882

LR026752

Giraldo and Crous (2019)

 

CBS 565.78B

Cercospora beticola

Moldavia

LR025883

LR026753

Giraldo and Crous (2019)

 

CBS 565.78C

Erysiphe sp.

Russia, Astrakhan

LR025884

LR026754

Giraldo and Crous (2019)

 

CBS 892.70T

Goldfish (Carassius auratus)

Brazil, Recife

LR025885

LR026755

Giraldo and Crous (2019)

 

CBS 100826

Solanum tuberosum

Israel, Gilat

LR025886

LR026756

Giraldo and Crous (2019)

 

CBS 100827

Soil in cotton field

Israel, Ramat-David

LR025887

LR026757

Giraldo and Crous (2019)

 

CBS 100830

Soil

Israel, Ein-Shemer

LR025888

LR026758

Giraldo and Crous (2019)

 

CBS 100831

Soil

Israel, Ein-Shemer

LR025889

LR026759

Giraldo and Crous (2019)

 

CBS 101221

Soil in cotton field

Israel, Ein-Shemer

LR025890

LR026760

Giraldo and Crous (2019)

 

CBS 109724

Human blood

Greece, Thessaloniki

LR025891

LR026761

Giraldo and Crous (2019)

 

CBS 120008

Leaf of Musa sp.

India, Bangoan, W.-Bengal

LR025892

LR026762

Giraldo and Crous (2019)

 

CBS 120177

Solanum tuberosum

Japan

LR025893

LR026763

Giraldo and Crous (2019)

 

JW 38004

Garden soil

The Netherlands, Sevenum

LR590365

LR590188

This study

 

JW 191018

Garden soil

The Netherlands, Amersfoort

LR590363

LR590186

This study

 

JW 234023

Garden soil

The Netherlands, Born

LR590364

LR590187

This study

G. simonii

JW 132008T = CBS 144923

Garden soil

The Netherlands, Gelderland, Meteren

MK047517

MK047467

LR594788

Crous et al. (2018), This study

 

JW 132005

Garden soil

The Netherlands, Gelderland, Meteren

LR590366

LR590189

LR594789

This study

Lectera capsici

CBS 142534T

Capsicum annuum

Malaysia

KY979825

KY979770

Crous et al. (2017a)

L. colletotrichoides

IMI 332702

Cicer arietinum

Egypt

LR025895

JQ647428

Cannon et al. (2012), Giraldo and Crous (2019)

L. humicola

IMI 265740T

Soil

Brazil

LR025896

JQ647449

Cannon et al. (2012), Giraldo and Crous (2019)

L. longa

IMI 181698T

Triticum sp.

Australia

LR025897

JQ647448

Cannon et al. (2012), Giraldo and Crous (2019)

L. nordwiniana

JW 46012 = CBS 144922

Garden soil

The Netherlands, Güeldres, Arnhem

MK047513

MK047463

MK047551

MK047572

Crous et al. (2018)

 

JW 231009T = CBS 144921

Garden soil

The Netherlands, Friesland, Leeuwarden

MK047511

MK047461

MK047549

MK047570

Crous et al. (2018)

 

JW 231013

Garden soil

The Netherlands, Friesland, Leeuwarden

MK047512

MK047462

MK047550

MK047571

Crous et al. (2018)

L. phaseoli

IMI 366179T

Phaseolus vulgaris

Ethiopia

LR025898

JQ693168

Cannon et al. (2012), Giraldo and Crous (2019)

Monilochaetes infuscans

CBS 379.77

Ipomoea batatas

New Zealand, South Auckland, Mangere

GU180645

LR026764

Réblová et al. (2011), Giraldo and Crous (2019)

 

CBS 869.66

Ipomoea batatas

South Africa, Eastern Cape, Gamtoos

GU180639

GU180626

Réblová et al. (2011)

Musidium stromaticum

CBS 135.74F

Rhizosphere of Musa sp.

Philippines

LR025925

LR026790

Giraldo and Crous (2019)

 

CBS 863.73T

Root and rhizome of Musa sapientum

Honduras

HQ232143

DQ825969

Summerbell et al. (2011), Zare et al. (2007)

Phialoparvum bifurcatum

CBS 299.70BT

Soil

Belgium, Heverlee

LR025931

LR026793

Giraldo and Crous (2019)

P. rietveltiae sp. nov.

JW 211005T = CBS 145322

Garden soil

The Netherlands, Utrecht

LR590367

LR590191

LR594790

This study

P. maaspleinense sp. nov.

JW 266001T = CBS 145321

Garden soil

The Netherlands, Utrecht

LR590368

LR590190

LR594791

This study

Plectosphaerella alismatis

CBS 113362ET

Alisma plantago-aquatica

The Netherlands, Pijnenburg near Soest

LR025932

LR026794

LR026489

Giraldo and Crous (2019)

P. citrullae

CBS 131740

Root of Cucumis melo

Italy, Foggia, Torre Bianca

LR025933

LR026795

LR026490

Giraldo and Crous (2019)

 

CBS 131741T

Root of Citrullus lanatus

Italy, Foggia

LR025934

LR026796

LR026491

Giraldo and Crous (2019)

P. cucumerina

CBS 137.33NT

Nicotiana tabacum

England, Bristol

LR025935

LR026797

LR026492

Giraldo and Crous (2019)

 

CBS 137.37T

Paper

Italy

LR025936

LR026798

LR026493

Giraldo and Crous (2019)

 

CBS 286.64

Nicotiana tabacum

Belgium, Heverlee

LR025938

LR026800

LR026495

Giraldo and Crous (2019)

 

CBS 355.36

Root of Viola tricolour

The Netherlands

LR025939

LR026801

LR026496

Giraldo and Crous (2019)

 

CBS 367.73

Viola odorata

Egypt

LR025940

LR026802

LR026497

Giraldo and Crous (2019)

 

CBS 400.58

Solanum esculentum

Canada

LR025941

LR026803

LR026498

Giraldo and Crous (2019)

 

CBS 619.74

Leaf of Pyrus malus

Switzerland, Basel

LR025943

LR026805

LR026500

Giraldo and Crous (2019)

 

CBS 101014

Arabidopsis thaliana

Switzerland

LR025945

LR026807

LR026502

Giraldo and Crous (2019)

 

CBS 101958

Endophyte in leaf and stem of Galium spurium

Canada, Alberta

LR025946

LR026808

LR026503

Giraldo and Crous (2019)

 

CBS 131739NT

Collar of Cucumis melo

Italy, Foggia, Borgo Cervaro

LR025947

LR026809

LR026504

Giraldo and Crous (2019)

 

JW 4021

Garden soil

The Netherlands, Breda

LR590375

LR590198

LR594792

This study

 

JW 29030

Garden soil

The Netherlands, Oude Wetering

LR590374

LR590197

LR594793

This study

 

JW 79002

Garden soil

The Netherlands, Kapel Avezaath

LR590376

LR590199

LR594794

This study

 

JW 79010

Garden soil

The Netherlands, Kapel Avezaath

LR590377

LR590200

This study

 

JW 144006

Garden soil

The Netherlands, Herten

LR590369

LR590192

This study

 

JW 144016

Garden soil

The Netherlands, Herten

LR590370

LR590193

This study

 

JW 198006

Garden soil

The Netherlands, Amsterdam

LR590371

LR590194

LR594795

This study

 

JW 236009

Garden soil

The Netherlands, Maasbracht

LR590372

LR590195

This study

 

JW 261010

Garden soil

The Netherlands, Utrecht

LR590373

LR590196

This study

P. delsorboi

CBS 116708T

Curcuma alismatifolia

Italy, Portici

LR025948

LR026810

LR026505

Giraldo and Crous (2019)

P. hanneae sp. nov.

JW181001T = CBS 144925

Garden soil

The Netherlands, Leiden

LR590378

LR590201

LR594767

This study

P. humicola

CBS 423.66T

Soil

Zaire, Katanga

LR025949

LR026811

LR026506

Giraldo and Crous (2019)

P. melonis

CBS 489.96T

Root of Cucurbita melo

Japan, Shizuoka, Asaba-chou

LR025950

LR026812

LR026507

_

Giraldo and Crous (2019)

 

CBS 525.93

Cucumis melo

Spain

LR025951

LR026813

LR026508

_

Giraldo and Crous (2019)

P. oligotrophica

CBS 440.90

Soil

Brazil, Pará

LR025952

LR026814

LR026509

Giraldo and Crous (2019)

P. oratosquillae

NJM 0662T

Mantis shrimp (Oratosquilla oratoria)

Japan, Yamaguchi

_

AB425974

_

_

Duc et al. (2009)

 

NJM 0665

Mantis shrimp (Oratosquilla oratoria)

Japan, Yamaguchi

_

AB425975

_

_

Duc et al. (2009)

P. pauciseptata

CBS 131744

Collar of Cucumis melo

Italy, Foggia

LR025953

LR026815

LR026510

_

Giraldo and Crous (2019)

 

CBS 131745T

Root of Solanum esculentum

Italy, Apulia, Rignano Garganico

LR025954

LR026816

LR026511

Giraldo and Crous (2019)

P. pauciseptata

JW 83023

Garden soil

The Netherlands, Ridderkerk

LR590379

LR590202

LR594768

LR594796

This study

P. plurivora

CBS 261.89

Soil

Germany

LR025958

LR026820

LR026515

Giraldo and Crous (2019)

 

CBS 292.66

Soil

The Netherlands

LR025960

LR026822

LR026517

Giraldo and Crous (2019)

 

CBS 386.68

Wheat field soil

The Netherlands, Oostelijk Flevoland

LR025961

LR026823

LR026518

Giraldo and Crous (2019)

 

CBS 131742T

Apex of Asparagus officinalis

Italy, Apulia, Borgo Cervaro

LR025967

LR026829

LR026524

Giraldo and Crous (2019)

 

JW 5012

Garden soil

The Netherlands, Nieuwegein

LR590412

LR590237

This study

 

JW 5035

Garden soil

The Netherlands, Nieuwegein

LR590413

LR590238

LR594769

LR594797

This study

 

JW 13024

Garden soil

The Netherlands, Alkmaar

LR590382

LR590205

LR594770

This study

 

JW 18012

Garden soil

The Netherlands, Valkenswaard

LR590391

LR590214

This study

 

JW 26001

Garden soil

The Netherlands, Soest

LR590399

LR590224

This study

 

JW 29002

Garden soil

The Netherlands, Oude Wetering

LR590401

LR590226

LR594771

LR594798

This study

 

JW 29017

Garden soil

The Netherlands, Oude Wetering

LR590402

LR590227

This study

 

JW 29025

Garden soil

The Netherlands, Oude Wetering

LR590403

LR590228

This study

 

JW 40004

Garden soil

The Netherlands, Goes

LR590404

LR590229

This study

 

JW 40005

Garden soil

The Netherlands, Goes

LR590405

LR590230

This study

 

JW 43013

Garden soil

The Netherlands, Zoelen

LR590406

LR590231

This study

 

JW 44009

Garden soil

The Netherlands, Utrecht

LR590407

LR590232

This study

 

JW 44018

Garden soil

The Netherlands, Utrecht

LR590408

LR590233

This study

 

JW 44021

Garden soil

The Netherlands, Utrecht

LR590409

LR590234

This study

 

JW 48008

Garden soil

The Netherlands, De Bilt

LR590410

LR590235

This study

 

JW 50045

Garden soil

The Netherlands, Houten

LR590411

LR590236

This study

 

JW 80004

Garden soil

The Netherlands, Geertruidenberg

LR590414

LR590239

This study

 

JW 124026

Garden soil

The Netherlands, Amersfoort

LR590380

LR590203

This study

 

JW 127008

Garden soil

The Netherlands, Utrecht

LR590381

LR590204

This study

 

JW 132001

Garden soil

The Netherlands, Meteren

LR590383

LR590206

This study

 

JW 137005

Garden soil

The Netherlands, Tilburg

LR590384

LR590207

This study

 

JW 141016

Garden soil

The Netherlands, Kortenhoef

LR590385

LR590208

This study

 

JW 144008

Garden soil

The Netherlands, Herten

LR590386

LR590209

This study

 

JW 146011

Garden soil

The Netherlands, Heemstede

LR590387

LR590210

This study

 

JW 152008

Garden soil

The Netherlands, Utrecht

LR590388

LR590211

This study

 

JW 154005

Garden soil

The Netherlands, De Meern

LR590389

LR590212

This study

 

JW 161013

Garden soil

The Netherlands, Utrecht

LR590390

LR590213

This study

 

JW 190001

Garden soil

The Netherlands, Wijk bij Duurstede

LR590392

LR590215

LR594772

LR594799

This study

 

JW 192005

Garden soil

The Netherlands, Woerden

LR590393

LR590216

This study

 

JW 198008

Garden soil

The Netherlands, Amsterdam

LR590394

LR590217

This study

 

JW 198019

Garden soil

The Netherlands, Amsterdam

LR590395

LR590218

This study

 

JW 200004

Garden soil

The Netherlands, Houten

LR590219

This study

 

JW 211020

Garden soil

The Netherlands, Utrecht

LR590396

LR590220

This study

 

JW 211027

Garden soil

The Netherlands, Utrecht

LR590397

LR590221

This study

 

JW 230016

Garden soil

The Netherlands, Maarssen

LR590398

LR590222

This study

 

JW 255003

Garden soil

The Netherlands, Ede

LR590223

LR594773

LR594800

This study

 

JW 266007

Garden soil

The Netherlands, Utrecht

LR590400

LR590225

This study

P. populi

CBS 139623T

Branch of Populus nigra

Germany, Kuestrin-Kietz, Brandenburg

KR476783

KR476750

LR026527

_

Crous et al. (2015) Giraldo and Crous (2019)

 

CBS 139624

Populus nigra

Germany, Kuestrin-Kietz, Brandenburg

MH878144

KR476751

LR026528

_

Crous et al. (2015), Giraldo and Crous (2019)

P. ramiseptata

CBS 131743

Collar of Citrullus lanatus

Italy, Foggia

LR025969

LR026831

LR026529

_

Giraldo and Crous (2019)

 

CBS 131861T

Root of Solanum esculentum

Italy, Apulia, Rignano Garganico

LR025970

LR026832

LR026530

_

Giraldo and Crous (2019)

P. sinensis

ACCC 39144

Stem of Citrullus lanatus

China, Hebei

KX527892

KX527889

_

_

Su et al. (2017)

 

ACCC 39145T

Stem of Cucumis melo

China, Hebei

KX527891

KX527888

_

_

Su et al. (2017)

P. verschoorii sp. nov.

JW 13004 = CBS 144924T

Garden soil

The Netherlands, Alkmaar

LR590476

LR590240

LR594774

_

This study

 

JW 13006

Garden soil

The Netherlands, Alkmaar

LR590415

LR590241

LR594775

LR594801

This study

 

JW 62006

Garden soil

The Netherlands, Delft

LR590426

LR590252

LR594776

LR594802

This study

 

JW 143005

Garden soil

The Netherlands, Utrecht

LR590416

LR590242

LR594777

LR594803

This study

 

JW 146007

Garden soil

The Netherlands, Heemstede

LR590417

LR590243

LR594778

_

This study

 

JW 146009

Garden soil

The Netherlands, Heemstede

LR590418

LR590244

LR594779

_

This study

 

JW 146016

Garden soil

The Netherlands, Heemstede

LR590419

LR590245

LR594780

_

This study

 

JW 150001

Garden soil

The Netherlands, Liempde

LR590420

LR590246

LR594781

_

This study

 

JW 170008

Garden soil

The Netherlands, Utrecht

LR590421

LR590247

LR594782

_

This study

 

JW 191043

Garden soil

The Netherlands, Amersfoort

LR590422

LR590248

LR594783

LR594804

This study

 

JW 208020

Garden soil

The Netherlands, Hilversum

LR590423

LR590249

LR594784

_

This study

 

JW 230011

Garden soil

The Netherlands, Maarssen

LR590424

LR590250

LR594785

LR594805

This study

 

JW 232007

Garden soil

The Netherlands, Nederweert

LR590425

LR590251

LR594786

LR594806

This study

ACCC, Agricultural Culture Collection of China, Beijing, China; CBS, Culture Collection of the Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands; DAOMC, Canadian Collection of Fungal Cultures, Canada; IMI, International Mycological Institute, CABI-Bioscience, Egham, Bakeham Lane, UK; JW, Johanna Westerdijk Culture Collection, Utrecht, The Netherlands; NJM, Nippon Veterinary and Life Science University, Tokyo, Japan; T, ex-type; ET, ex-epitype; IT, ex-isotype; NT, ex-neotype; ENA, European Nucleotide Archive; LSU, large subunit of the nrDNA; ITS, internal transcribed spacer regions of the nrDNA and intervening 5.8S nrDNA; TEF1-α, translation elongation factor 1-alpha; RPB2, RNA polymerase II second largest subunit. Accession numbers of sequences generated in this study are in bold

Phylogenetic analysis

Sequences were aligned through MAFFT v. 7 (Katoh et al. 2017), using the default parameters, and were manually corrected in MEGA v. 6.06 (Tamura et al. 2013). Phylogenetic inferences of the individual gene regions and the combined dataset were based on maximum likelihood (ML) and were performed on the CIPRES Science Gateway portal (Miller et al. 2012) using RAxML v. 8.2.10 (Stamatakis, 2014). The default parameters were used, and bootstrap support (BS) was carried out using the rapid bootstrapping algorithm with the automatic halt option. A BS ≥ 70% was considered as statistically significant. Each partition was assessed for incongruence before being concatenated by checking individual phylogenies for conflicts between clades with significant ML support (Mason-Gamer and Kellogg 1996; Wiens 1998). All novel DNA sequences generated in this study were deposited in GenBank and ENA databases (Table 1), while the alignments and the resulting trees were accessioned in TreeBASE (http://www.treebase.org).

Morphological characterisation of novel species

Morphological features from the new species were determined on oatmeal agar (OA), potato carrot agar (PCA), 2% potato dextrose agar (PDA) and 2% malt extract agar (MEA) (recipes in Crous et al. 2019). Cultures were incubated at ca. 24 °C in the dark for 4 weeks. Macroscopic characters and diameters were measured after 14 days of incubation, and the colony colour (surface and reverse) rated after Rayner (1970). Microscopic features were examined from slide cultures and preparations mounted in clear lactic acid from colonies sporulating on the media previously mentioned. Observations were performed with a Zeiss V20 Discovery (Zeiss, Oberkochen, Germany) stereo microscope and with a Zeiss Axio Imager 2 light microscope using differential interference contrast (DIC) optics. Photomicrographs and measurements were taken with a Nikon DS-Ri2 digital camera (Nikon, Tokyo, Japan) using the NIS-elements imaging software v. 4.3. The length and width of at least 30 randomly selected structures were measured, and the extreme values calculated. Morphological descriptions and taxonomic information for the new species were deposited in MycoBank (www.MycoBank.org; Crous et al. 2004).

Results

A total of 293 soil samples were analysed, and nearly 3000 fungal isolates were obtained. Among them, 176 were identified as members of Plectosphaerellaceae according to the BLAST search results using the LSU and/or ITS sequences. The combined ITS and LSU dataset comprises 197 sequences including the ones generated in the present study from soil isolates, together with reference sequences of Plectosphaerellaceae taxa download from GenBank, and the outgroup Monilochaetes infuscans CBS 379.77 and CBS 869.96 (Fig. 1). The RAxML tree showed BS values higher than 95% for all the generic clades, except for Gibellulopsis and Brunneochlamydosporum that were not fully supported (Fig. 1). The majority of the isolates were distributed among Plectosphaerella spp. (n = 61) and Gibellulopsis spp. (n = 60). They were followed by Chordomyces spp. (n = 22), Acrostalagmus luteoalbus (n = 15) and Brunneochlamydosporium spp. (n = 9). The remaining isolates were identified as Furcasterigmium furcatum (n = 4), Lectera nordwiniana (n = 3) and Phialoparvum spp. (n = 2) (Table 1). Since the species boundaries were not resolved with this analysis for Brunneochlamydosporium, Chordomyces, Gibellulopsis, Phialoparvum and Plectosphaerella, subsequent phylogenetic analyses were carried out (Figs. 2, 3, 4 and 5).
Fig. 1

Maximum composite likelihood tree based on partial sequences from the ITS and LSU from all the soil isolates placed in Plectosphaerellaceae. Colour boxes indicate the generic clade. Bootstrap support values above 70% are shown at the genus nodes (internal values are not shown). TEx-type, ITEx-isotype, NTEx-neotype

Fig. 2

Maximum composite likelihood tree based on ITS and TEF1-α from Brunneochlamydosporium species. Colour boxes indicate the generic clade. Bootstrap support values above 70% are shown at the nodes. JW isolates are in green font and the ex-type strains in bold. TEx-type, ITEx-isotype

Fig. 3

Maximum composite likelihood tree based on ITS from Chordomyces, Lectera and Phialoparvum species. Colour boxes indicate the generic clade. Bootstrap support values above 70% are shown at the nodes. JW isolates are in green font and the ex-type strains in bold. TEx-type

Fig. 4

Maximum composite likelihood tree based on partial sequences from ITS from Gibellulopsis species. Colour boxes indicate the generic clade. Bootstrap support values above 70% are shown at the nodes. JW isolates are in green font and the ex-type strains in bold. TEx-type

Fig. 5

Maximum composite likelihood tree based on ITS and TEF1-α from Plectosphaerella species. Colour boxes indicate the generic clade. Bootstrap support values above 70% are shown at the nodes. JW isolates are in green font and the ex-type strains in bold. TEx-type, ETEx-epitype, NTEx-neotype

The Brunneochlamydosporium dataset comprises ITS and TEF1-α sequences of 19 isolates including the outgroups (Fig. 2). This combined analysis showed B. nepalense (n = 7) as the most common species, followed by B. macroclavatum (n = 1). The ITS phylogeny represented in Fig. 3 shows the species distribution from all the isolates belonging to Chordomyces, Lectera and Phialoparvum. In the Chordomyces clade (95% BS), most of the isolates (n = 17) were grouped with the type of C. albus CBS 987.87 (76%), while the remaining isolates (n = 5) were identified as C. antarticus. The three isolates of Lectera were confirmed as L. nordwiniana, but the two Phialoparvum isolates were genetically different from the type of Ph. bifurcatum CBS 299.70B, representing two putative new species, introduced in the ‘Taxonomy’ section.

The phylogenetic analysis shown in Fig. 4 encompasses the ITS sequences from 106 isolates belonging to Gibellulopsis (including the ex-type strains from the different Gibellulopsis species), and Furcasterigmium and Musidium as outgroups (Fig. 4). According to this phylogeny, the majority of the soil isolates were identified as G. nigrescens (n = 50), followed by G. fusca (n = 5), G. serrae (formerly G. piscis) (n = 3) and G. simonii (n = 2).

A preliminary phylogenetic analysis based on the ITS region was carried out for Plectosphaerella (data not shown). Species were distributed in Pl. plurivora (n = 37), Pl. cucumerina (n = 9) and Pl. pauciseptata (n = 1) (Table 1). However, 14 isolates were distributed in two different lineages (with 1 and 13 isolates, respectively), phylogenetically distant from the other species. Subsequently, isolates of each clade were selected based in the similarity of their ITS regions for further combined analysis of ITS and TEF1-α sequences. This analysis included 55 soil isolates and 32 reference strains (Fig. 5), and confirmed the identity of the isolates placed in the Pl. plurivora (77% BS) and Pl. cucumerina clades (88% BS). Furthermore, this analysis revealed that 13 isolates were nested in a highly supported clade (99% BS), phylogenetically distant from the remaining species in the genus, representing a potentially new species. Isolate JW 181001 was placed in a single branch related (71% BS) but different from Pl. alismatis, Pl. delsorboi, Pl. melonis and Pl. sinensis. The two new species are described in the ‘Taxonomy’ section below.

Taxonomy

Based on the molecular results and the morphological observations, four new species are described and illustrated here, i.e. Phialoparvum maaspleinense, Ph. rietveltiae, Plectosphaerella hanneae and Pl. verschoorii.

Phialoparvum maaspleinense Hern.-Restr. & Giraldo López, sp. nov. MycoBank MB 831346 (Fig. 6a, b, e–j).
Fig. 6

Phialoparvum spp. a, b, ejPhialoparvum maaspleinense (ex-type CBS 145321 = JW 266001). a, b Colonies on PDA and MEA respectively, after 14 days at ca. 24 °C. e, f Monophialides and conidia. g Polyphialide and conidium. h, i Adelophialides and conidia. j Conidia. c, d, knPhialoparvum rietveltiae (ex-type CBS 145322 = JW 211005). c, d Colonies on PDA and MEA respectively, after 14 days at ca. 24 °C. k Monophialides and conidia. l Polyphialides and conidia. m Adelophialide. n Conidia. Scale bars: gi, m = 5 μm. e, f, jl, n = 10 μm

Etymology. Named after ‘Maaspleinschool’ from Utrecht, where the soil sample was collected by the students Ouail Zaim and Mohamed Bidari.

Mycelium consisting of branched, septate, smooth, hyaline and thick-walled hyphae, 1.5–2.5 μm wide. Conidiophores solitary, erect, arising directly from vegetative hyphae or ropes of hyphae, unbranched or poorly branched. Phialides lateral, terminal, subulate, hyaline, thick- and smooth-walled, 10–42 × 1.5–3 μm, with cylindrical collarette and conspicuous periclinal thickening at the conidiogenous locus; adelophialides commonly present, intercalary and terminal, up to 4 μm long; polyphialides with two conidiogenous loci are commonly present. Conidia arranged in slimy heads, cylindrical, sometimes with slightly truncate base, 1-celled, hyaline, thick- and smooth-walled, 3.5–5 × 2 μm. Sexual morph unknown.

Culture characteristics — After 14 days at ca. 24 °C on PDA reaching 45–48 mm diam., flat, membranous, aerial mycelium sparse, dirty white, reverse uncoloured. On OA reaching 40–42 mm diam., flat, pulverulent, rosy buff, margin effuse, reverse buff to honey. On MEA reaching 37–38 mm diam., radially folded, velvety at centre, pulverulent toward the periphery, dirty white, margin entire, reverse uncoloured.

Typus. The Netherlands, Utrecht province, Utrecht, Maaspleinschool, from garden soil, 2017, coll. O. Zaim & M. Bidari, isol. A. Giraldo (holotype CBS H-23910, cultures ex-type CBS 145321 = JW 266001).

Notes: The monotypic genus Phialoparvum was recently proposed based on Ph. bifurcatum, recovered from soil in Belgium (Giraldo and Crous 2019). Phialoparvum bifurcatum and the new species, Ph. maaspleinense can be morphologically distinguished based on phialide length (up to 15 μm in Ph. bifurcatum vs up to 42 μm in Ph. maaspleinense; Giraldo and Crous 2019) and the frequent production of intercalary and terminal adelophialides in the latter species (Fig. 6h, i).

Phialoparvum rietveltiae Hern.-Restr. & Giraldo López, sp. nov. MycoBank MB 831347 (Fig. 6c, d, k–n).

Etymology. Named after Emma Rietvelt, who collected the soil sample.

Mycelium consisting of branched, septate, hyaline and thick-walled hyphae, 1–2 μm wide. Conidiophores solitary, erect, arising directly from vegetative hyphae or ropes of hyphae, unbranched or poorly branched. Phialides lateral, terminal, subulate to ampulliform, hyaline, thick- and smooth-walled, 6–11(− 17) × 1–2.5 μm, with cylindrical collarette and conspicuous periclinal thickening at the conidiogenous locus, adelophialides sometimes present, up to 4 μm long; polyphialides with two conidiogenous loci are commonly present. Conidia arranged in slimy heads, cylindrical, with slightly pointed ends, 1-celled, hyaline, thick- and smooth-walled, 3.5–5 × 1.5–2 μm. Sexual morph unknown.

Culture characteristics — After 14 days at ca. 24 °C on PDA reaching 30–33 mm diam., flat, membranous, aerial mycelium sparse or absent, dirty white, margin entire, reverse uncoloured. On OA reaching 28–30 mm diam., flat, pulverulent to velvety, dirty white to buff, margin rhizoid, reverse uncoloured. On MEA reaching 24–29 mm diam., umbonate, radially folded, membranous to felty, buff, entire margin, reverse uncoloured.

Typus. The Netherlands, Utrecht province, Utrecht, from garden soil, 2017, coll. E. Rietvelt, isol. A. Giraldo (holotype CBS H-23911, cultures ex-type CBS 145322 = JW 211005).

Notes: Phialoparvum bifurcatum and Ph. rietveltiae are morphologically similar in phialide shape and length (8–15 μm in Ph. bifurcatum vs 6–17 μm in Ph. rietveltiae). However, the latter species has longer conidia (3.5–5 μm in Ph. rietveltiae vs 2.8–4.4 μm in Ph. bifurcatum) and does not produce melanin precipitations in culture (Giraldo and Crous 2019).

Plectosphaerella hanneae Giraldo López & Hern.-Restr., sp. nov. MycoBank MB 831348 (Fig. 7a–d).
Fig. 7

Plectosphaerella spp. adPlectosphaerella hanneae (ex-type CBS 144925 = JW 181001). a Colony on PDA after 14 days at ca. 24 °C. b Monophialide and conidia. c Monophialides with a percurrent proliferation (arrow) and conidia. d Septate and aseptate conidia. eiPlectosphaerella verschoorii (ex-type CBS 144924 = JW 13004). e Colony on PDA after 14 days at ca. 24 °C. f Monophialides and conidia. g Adelophialide and conidia. h, i Septate and aseptate conidia. Scale bars = 10 μm

Etymology. Named after Hanne de Levita, who collected the soil sample.

Mycelium consisting of branched, septate, smooth, hyaline and thin-walled hyphae, up to 2 μm wide. Conidiophores solitary, erect, unbranched, hyaline, smooth-walled, sometimes radiating out from sterile coils formed by the mycelium. Phialides lateral or terminal, subulate, hyaline, smooth- and thick-walled, occasionally borne on short cylindrical subtending cells, 16–32 × 2–4.5 μm, with conspicuous cylindrical collarette and periclinal thickening at the conidiogenous locus, sometimes with percurrent proliferation; adelophialides rarely present, up to 15 μm long. Conidia arranged in slimy heads, (0-)1-septate, cylindrical to ellipsoidal with pointed apex and slightly truncate base, inequilateral, with inner plane flat and outer plane convex, guttulate, hyaline, thin- and smooth-walled; septate conidia abundant, 9–12.5 × 2.5–3.5 μm; aseptate conidia scarce, 9–10.5 × 3–3.5 μm. Chlamydospores and sexual morph absent.

Culture characteristics — After 14 days at ca. 24 °C on PDA reaching 76–77 mm diam., flat, membranous, dirty white to pale luteous, aerial mycelium sparse or absent, with concentric rings, reverse uncoloured. On OA reaching 58–60 mm diam., flat, glabrous, pale luteous with ochreous border, aerial mycelium sparse at the periphery, reverse uncoloured.

Typus. The Netherlands, South Holland, Leiden, from garden soil, 2017, coll. H. de Levita, isol. A. Giraldo (holotype CBS H-23737, cultures ex-type CBS 144925 = JW 181001).

Notes: According to phylogenetic inference from the ITS and TEF1-α loci (Fig. 5), Pl. hanneae occupies a single branch in the clade containing Pl. alismatis, Pl. delsorboi, Pl. melonis and Pl. sinensis (71% BS). With the exception of Pl. delsorboi and Pl. hanneae, all the species in that clade produce hyaline chlamydospores in chains (Su et al. 2017). Plectosphaerella delsorboi differs in having longer phialides (30–50 μm; Antignani et al. 2008) than those of Pl. hanneae (16–32 μm).

Plectosphaerella verschoorii Giraldo López & Hern.-Restr., sp. nov. MycoBank MB 831349 (Fig. 7e–i).

Etymology. Named after Brent Verschoor, who collected the soil sample.

Mycelium consisting of branched, septate, smooth, hyaline and thin-walled hyphae, up to 2 μm wide. Conidiophores solitary, erect, unbranched or poorly branched, hyaline, smooth-walled. Phialides lateral or terminal, subcylindrical to subulate, hyaline, smooth- and thick-walled, 16–29 × 1.5–3 μm, with conspicuous cylindrical collarette and periclinal thickening at the conidiogenous locus; adelophialides, rarely present; ampulliform, up to 14 μm long. Conidia arranged in slimy head, (0-)1-septate, cylindrical to ellipsoidal with pointed apex and slightly truncate base, or broadly ellipsoidal, guttulate, hyaline, thin- and smooth-walled; septate conidia abundant, sometimes slightly constricted at the septum, 8–11.5 × 2–3 μm; aseptate conidia scarce, 3–8.5 × 2–3 μm. Chlamydospores and sexual morph absent.

Culture characteristics — After 14 days at ca. 24 °C on PDA reaching 76–77 mm diam., flat, membranous, flesh at centre, pale luteous at periphery, aerial mycelium sparse, with concentric rings, dirty white, reverse uncoloured. On OA reaching 70–75 mm diam., flat, glabrous, honey, reverse uncoloured.

Typus. The Netherlands, North Holland, Alkmaar, from garden soil, 2017, coll. B. Verschoor, isol. A. Giraldo (holotype CBS H-23738, cultures ex-type CBS 144924 = JW 13004).

Additional specimens examined: The Netherlands, Limburg, Nederweert, from garden soil, 2017, coll. M. van Meijl, isol. A. Giraldo, JW 232007; North Brabant, Liempde, from garden soil, 2017, coll. L. & V. Gijzen, isol. A. Giraldo, JW 150001; North Holland, Alkmaar, from garden soil, 2017, coll. Brent Verschoor, isol. A. Giraldo, JW 13006; Heemstede, from garden soil, 2017, coll. Alfons Vaessen, isol. A. Giraldo, JW 146007, JW 146009, JW 146016; Hilversum, from garden soil, 2017, coll. J.A.L. Keyes-Rens, isol. A. Giraldo, JW 208020; South Holland, Delft, from garden soil, 2017, E. & M. Bordes, isol. A. Giraldo, JW 62006; Utrecht, Amersfoort, from garden soil, 2017, coll. T. & K. Wesselink, isol. A. Giraldo, JW 191043; Maarssen, from garden soil, 2017, coll. Y. & F. van der Ouderaa, isol. A. Giraldo, JW 230011; Utrecht, from garden soil, 2017, coll. G. Bleijlevens, isol. A. Giraldo, JW 143005; from garden soil, 2017, coll. J.P. van Eesteren, isol. A. Giraldo, JW 170008.

Notes: Plectosphaerella verschoorii forms a well-supported clade (99% BS, Fig. 5), phylogenetically different from other Plectosphaerella species. This species was collected in five provinces from The Netherlands (i.e. Limburg, North Brabant, North and South Holland, and Utrecht).

Morphologically, Plectosphaerella verschoorii resembles Pl. citrullae, Pl. delsorboi, Pl. hanneae and Pl. plurivora in lacking polyphialides. However, it can be distinguished from Pl. plurivora by the scarce production of aseptate conidia; from Pl. delsorboi and Pl. citrullae by having shorter phialides (up to 29 μm in Pl. verschoorii, up to 50 μm in Pl. delsorboi, up to 60 μm in Pl. citrullae; Carlucci et al. 2012; Liu et al. 2013), and from Pl. hanneae by producing smaller aseptate conidia (3–8.5 × 2–3 μm in Pl. verschoorii vs. 9–10.5 × 3–3.5 μm in Pl. hanneae, this study).

Discussion

Although there are no specific studies exploring the diversity of the plectosphaerellaceous species from soil, a survey about fungi from soda soils in Asia (Armenia, Kazakhstan, Mongolia and Russia) and Africa (Kenia and Tanzania) revealed several isolates representing four genera of Plectosphaerellaceae (Grum-Grzhimaylo et al. 2016). That study showed Sodiomyces spp. and A. luteoalbus as obligate and facultative alkaliphilic fungi, respectively, while C. antarticus and V. zaregamsianum seemed to be alkalitolerant species. In our set of samples, we did not find Sodiomyces spp. nor V. zaregamsianum, probably due of the media used for primary isolation. However, in our study, A. luteoalbus and C. antarticus were represented by 13 and five isolates respectively (Figs. 1 and 3 and Table 1). Additionally, we obtained several isolates (n = 17) of C. albus, which was recently described from a lichen (Hypogymnia physodes) and human sputum (Giraldo et al. 2017), but also reported from soil in Belgium, France, Germany and the Netherlands (Giraldo and Crous 2019).

In addition, we have identified several isolates from genera recently added to Plectosphaerellaceae, i.e. Brunneochlamydosporium, Furcasterigmium, Lectera and Phialoparvum (Cannon et al. 2012; Giraldo and Crous 2019). Brunneochlamydosporium was proposed to accommodate Acremonium nepalense, Gliocladium cibotii and the new species B. macroclavatum and B. terrestre. Brunneochlamydosporium nepalense and B. macroclavatum were represented in our study with seven and one isolate respectively. According to Prenafeta-Boldú et al. (2014), the former species seems to be a common soil-borne fungus in the Netherlands, being present in Gelderland, North and South Holland and Utrecht provinces, while B. macroclavatum was isolated from a fern, and the flowering plant, Aphelandra sp. (Acanthaceae), but not from soil (Giraldo and Crous 2019).

Furcasterigmium furcatum was established based on Acremonium furcatum, and it was represented in our study with four isolates collected from North Brabant, South Holland and Utrecht provinces. Like B. nepalense, this species was recovered from soil in the Netherlands, but is also present in soils from France, Germany and Italy (Gams 1971; Giraldo and Crous 2019).

Two soil samples of Friesland and Gederland provinces revealed three isolates of Lectera that turned out to represent the new species, L. nordwiniana (Crous et al. 2018). Although most of the species in Lectera are plant pathogens, including L. colletotrichoides and L. capsici (Crous et al. 2017a), the former species is commonly isolated from soil and plant litter (Cannon et al. 2012). Another species recently described from soil is L. humicola from Brazil (Giraldo and Crous 2019).

In this study, Gibellulopsis and Plectosphaerella were the dominant genera, with G. nigrescens and Pl. plurivora as the most common species from each respective genus. In some studies of fungal biodiversity in soil, Gibellulopsis and Plectosphaerella are occasionally recovered (Hujslová et al. 2010; Duran et al. 2019; Wentzel et al. 2019). According to the data shown by Giraldo and Crous (2019), Gibellulopsis spp. inhabit soils around the world, with G. nigrescens recovered from Israel, the Netherlands, New Zealand and the UK. Species of Plectosphaerella are more common on plants than in soil, except for Pl. plurivora, which is present in soils of different countries in Northern Europe (Belgium, the Netherlands and Germany), and Pl. humicola and Pl. oligotrophica from Democratic Republic of the Congo, Brazil and China, respectively (Liu et al. 2013; Giraldo and Crous 2019). In our study, a single isolate (JW 83023) was identified as Pl. pauciseptata, known thus far from Citrullus lanatus, Cucumis melo, C. sativus and Solanum esculetum in Italy (Carlucci et al. 2012). Therefore, this is the first time that this species has been recovered from soil.

Other studies have described G. nigrescens from soil samples in Korea (Nguyen et al. 2018) and China (Wu et al. 2013), where it was also shown to be the cause of wilt of sugar beet (Zhou et al. 2017) and alfalfa (Hu et al. 2011). In Europe, this species and Plectosphaerella spp. have been found in saline and acidic soils in the Czech Republic (Hujslová et al. 2010), and inhabiting in good quality soils (as Gleyic Chernozem, Fluvic Cambisol, Cambic Leptosol) in Poland (Grządziel and Gałązka 2019). In a survey about microfungal community in cultivated soils, Pl. cucumerina and A. luteoalbus (as Verticillium tenerum) were found in low proportions in soils from different locations of the Eskişehir province in Turkey (Demirel et al. 2005). In Argentina, Pl. plurivora was found in rhizosphere soil, showing an antagonistic effect against eggs of the plant-parasitic nematode Nacobbus aberrans (Sosa et al. 2018), and Plectosphaerella sp. was recovered from farmland in the Tibetan Plateau (Li et al. 2012).

The studies based in Next Generation Sequence generally show a higher diversity of soil fungi compared with those based on culture-dependent methods (Tedersoo et al. 2014, 2017; Wardle and Lindahl 2014). The latter approach usually overlooks the true diversity, mainly because of the low percentage of fungi growing on artificial media. However, through this Citizen science project, we have explored the fungal diversity of Dutch soils, which has revealed a rich species diversity. Some of the taxa obtained represent new species, genera and even families, which have been described here or in other publications (Crous et al. 2017b, 2018; Groenewald et al. 2018), while others are still awaiting description (unpubl. data). As a result of this project, around 3000 fungal isolates were obtained from 293 soil samples. Among them, 386 isolates were yeast fungi which were treated by Groenewald et al. (2018), who identified 67 species distributed over 40 genera (including basidiomycetous and ascomycetous) including six new species in the genera Hanseniaspora, Ogataea, Pichia, Saccharomycopsis, Trichomonascus and Zygoascus. Regarding filamentous fungi, new taxa have been described in different and unrelated genera, including Acaulium, Collariella, Conioscypha, Fusarium, Fusicolla, Gamsia, Gibellulopsis, Lasionectria, Lectera, Leptodiscella, Parasarocladium, Phaeoisaria, Sarocladium, Striaticonidium, Talaromyces, Umbelopsis, Vandijckella (incl. Vandijckella gen. nov. and Vandijckellaceae fam.nov.) and Verhulstia trisororum (incl. Verhulstia gen. nov.). These results support previous findings concluding that soil contains numerous undescribed fungal taxa (Hujslová et al. 2010; Tedersoo et al. 2014, 2017; Wentzel et al. 2019) and highlights the importance to continue with these kinds of studies in order to generate isolates that can be available in public databases and can be freely used by other researchers.

Notes

Acknowledgements

We are grateful to all the children, parents and teachers that enthusiastically participated in the collecting and submission of samples to the Westerdijk Institute. We are thankful to the Utrecht University Museum and KNAW for funding and promoting the project among the Dutch primary schools; to the Utrecht University for coordinating the initiative ‘meet the professor’; to the staff from the Westerdijk Institute: Manon Verweij, Karin Schagen and Mariëtte Oosterwegel for promoting the project and establishing communication with the collectors and schools. We also thank the CBS collection staff, especially Trix Merkx and Arien van Iperen for depositing the isolates and specimens in the culture collection and fungarium. Additional thanks are extended to the MycoBank curator, Konstanze Bench, for her suggestions and for checking the spelling of the epithets of the new species, and Duong Vu for her assistance with the database.

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© The Author(s) 2019

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  1. 1.Westerdijk Fungal Biodiversity InstituteUtrechtThe Netherlands
  2. 2.Faculty of Natural and Agricultural Sciences, Department of Plant SciencesUniversity of the Free StateBloemfonteinSouth Africa
  3. 3.Microbiology, Department of BiologyUtrecht UniversityUtrechtThe Netherlands

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