Research Article |
Corresponding author: Xiao-Yong Liu ( liuxiaoyong@im.ac.cn ) Corresponding author: Bo Huang ( bhuang@ahau.edu.cn ) Academic editor: Marc Stadler
© 2020 Yong Nie, De-Shui Yu, Cheng-Fang Wang, Xiao-Yong Liu, Bo Huang.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Nie Y, Yu D-S, Wang C-F, Liu X-Y, Huang B (2020) A taxonomic revision of the genus Conidiobolus (Ancylistaceae, Entomophthorales): four clades including three new genera. MycoKeys 66: 55-81. https://doi.org/10.3897/mycokeys.66.46575
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The genus Conidiobolus is an important group in entomophthoroid fungi and is considered to be polyphyletic in recent molecular phylogenies. To re-evaluate and delimit this genus, multi-locus phylogenetic analyses were performed using the large and small subunits of nuclear ribosomal DNA (nucLSU and nucSSU), the small subunit of the mitochondrial ribosomal DNA (mtSSU) and the translation elongation factor 1-alpha (EF-1α). The results indicated that the Conidiobolus is not monophyletic, being grouped into a paraphyletic grade with four clades. Consequently, the well-known Conidiobolus is revised and three new genera Capillidium, Microconidiobolus and Neoconidiobolus are proposed along with one new record and 22 new combinations. In addition, the genus Basidiobolus is found to be basal to the other entomophthoroid taxa and the genus Batkoa locates in the Entomophthoraceae clade.
Zygomycetes, Entomophthorales, Morphology, Phylogeny, New taxa
More than 250 species of entomophthoroid fungi were isolated from insects, soil and litter throughout the world (
Together with other two genera Ancylistes and Macrobiotophthora, the genus Conidiobolus belongs to Ancylistaceae, Entomophthorales, Entomophthoromycetes, Entomophthoromycotina (Humber 2012). There are six and two accepted species within the Ancylistes and Macrobiotophthora, respectively, while Conidiobolus, one of the largest groups in the entomophthoroid fungi, contains 76 names (http://www.indexfungorum.org/). The genus Conidiobolus is typified by C. utriculosus Bref. 1884 and characterised morphologically by simple sporophores, globose to pyriform multinucleate primary conidia, various types of secondary conidia and resting spores (
Three subgenera – Capillidium, Conidiobolus and Delacroixia – were proposed within the Conidiobolus, based on shape of the secondary conidia and, amongst them, the subgenus Delacroixia was reduced from generic rank (
In the present study, a reclassification of the entomophthoroid fungi, including as many as available Conidiobolus types, was constructed based on four loci (nucSSU, nucLSU, EF-1α and mtSSU) to present the taxonomic delimitation of the genus Conidiobolus and to re-evaluate the phylogenetic relationship between Basidiobolus and Batkoa.
A total of 26 ex-types of Conidiobolus were purchased from the American Type Culture Collection, Manassas, USA (
Fungal strains were incubated on PDA for 7 d at 21 °C. Total genomic DNA was extracted from the fresh fungal mycelia by using modified CTAB method (
Species | Strains* | GenBank accession numbers | |||
---|---|---|---|---|---|
nucSSU | nucLSU | EF-1α | mtSSU | ||
Allomyces arbusculus | AFTOL 300 | AY552524 | DQ273806 | DQ275334 | – |
Basidiobolus haptosporus | ARSEF 261 | JX242606 | JX242586 | – | JX242626 |
B. heterosporus | CBS 311.66 | JX242607 | JX242587 | – | JX242627 |
B. magnus | CBS 205.64 | JX242608 | JX242588 | – | JX242628 |
B. meristosporus | CBS 931.73 | JX242609 | JX242589 | – | JX242629 |
B. microsporus | CBS 130.62 (T) | JX242610 | JX242590 | – | JX242630 |
B. ranarum | NRRL 34594 | AY635841 | DQ273807 | DQ275340 | EF392490 |
Batkoa apiculata | ARSEF 3130 | DQ177437 | EF392404 | – | EF392513 |
B. gigantea | ARSEF 214 | JX242611 | JX242591 | – | JX242631 |
B. major | ARSEF 2936 | EF392559 | EF392401 | – | EF392511 |
B. obscurus** | CBS 182.60 | JX242614 | JX242595 | – | JX242635 |
B. pseudapiculata** | ARSEF 395 | EF392557 | EF392378 | – | EF392508 |
Coemansia reversa | AFTOL 140 | AY546685 | AY546689 | DQ282615 | – |
Conidiobolus adiaeretus | ARSEF 451 (T) | – | KC461182 | – | – |
C. adiaeretus |
|
– | MN061284 | MN061481 | MN061287 |
C. antarcticus | ARSEF 6913 (T) | – | DQ364207 | – | DQ364227 |
C. bangalorensis | ARSEF 449 (T) | – | DQ364204 | – | DQ364225 |
C. brefeldianus | ARSEF 452 (T) | AF368506 | EF392382 | – | EF392495 |
C. chlamydosporus |
|
– | JF816212 | JF816234 | MK301178 |
C. coronatus | NRRL 28638 | AF113418 | AY546691 | DQ275337 | – |
C. coronatus |
|
– | JN131537 | JN131543 | – |
C. couchii |
|
– | JN131538 | JN131544 | MK301179 |
C. dabieshanensis |
|
– | KY398125 | KY402206 | MK301180 |
C. denaeosporus |
|
– | JF816215 | JF816228 | MK301181 |
C. firmipilleus | ARSEF 6384 | JX242612 | JX242592 | – | JX242632 |
C. gonimodes |
|
– | JF816221 | JF816226 | MK301182 |
C. heterosporus |
|
– | JF816225 | JF816239 | MK301183 |
C. humicolus |
|
– | JF816220 | JF816231 | MK301184 |
C. incongruus | NRRL 28636 | AF113419 | AF113457 | – | – |
C. iuxtagenitus | ARSEF 6378 (T) | – | KC788410 | – | – |
C. iuxtagenitus |
|
– | JX946695 | JX946700 | MK333391 |
C. khandalensis |
|
– | KX686994 | KY402204 | MK301185 |
C. lachnodes | ARSEF 700 | – | KC788408 | – | – |
C. lamprauges | ARSEF 2338 | AF296754 | DQ364206 | – | DQ364226 |
C. lichenicolus |
|
– | JF816216 | JF816232 | MK301186 |
C. lobatus |
|
– | JF816218 | JF816233 | MK301187 |
C. marcosporus |
|
– | KY398124 | KY402209 | MK301188 |
C. megalotocus |
|
– | MF616383 | MF616385 | MK301189 |
C. mirabilis |
|
– | MH282852 | MH282853 | MK333389 |
C. mycophagus |
|
– | JX946694 | JX946698 | MK301190 |
C. mycophilus |
|
– | KX686995 | KY402205 | MK301191 |
C. nodosus |
|
– | JF816217 | JF816235 | MK333388 |
C. osmodes | ARSEF 79 | AF368510 | EF392371 | – | DQ364219 |
C. osmodes | RCEF4447 | – | JN131539 | JN131545 | MK333392 |
C. pachyzygosporus |
|
– | KP218521 | KP218524 | MK333390 |
C. paulus | ARSEF 450 (T) | – | vv | – | – |
C. polyspermus |
|
– | MF616382 | MF616384 | MK301193 |
C. polytocus |
|
– | JF816213 | JF816227 | MK301194 |
C. pumilus | ARSEF 453 (T) | JX242615 | EF392383 | – | EF392496 |
C. rhysosporus |
|
– | JN131540 | JN131546 | MK301195 |
C. sinensis |
|
– | JF816224 | JF816238 | MK301196 |
C. stilbeus |
|
– | KP218522 | KP218525 | MK301197 |
C. stromoideus |
|
– | JF816219 | JF816229 | MK301198 |
C. terrestris |
|
– | KX752050 | KY402208 | MK301199 |
C. thromboides |
|
– | JF816214 | JF816230 | MK301200 |
C. thromboides |
|
JX242616 | JX242597 | – | JX242637 |
C. thromboides |
|
– | JF816223 | JF816236 | MK333393 |
C. undulatus |
|
– | JX946693 | JX946699 | MK301201 |
Dimargaris bacillispora | AFTOL 136 | AB016020 | DQ273791 | DQ282609 | – |
Endogone pisiformis | AFTOL 539 | DQ322628 | DQ273811 | DQ282618 | – |
Entomophaga aulicae | ARSEF 172 | EF392542 | EF392372 | – | EF392487 |
E. conglomerata | ARSEF 2273 | AF368509 | – | – | – |
E. maimaga | ARSEF 1400 | EF392556 | EF392395 | – | EF392505 |
Eryniopsis caroloniana | ARSEF 640 | EF392552 | EF392387 | – | EF392500 |
Entomophthora chromaphidis | ARSEF 1860 | AF353725 | – | – | – |
E. culicis | ARSEF 387 | AF368516 | – | – | – |
E. grandis | ARSEF 6701 | – | DQ481229 | – | – |
E. scatophaga | ARSEF 6704 | – | DQ481226 | – | – |
E. muscae | ARSEF 3074 | AY635820 | DQ273772 | DQ275343 | – |
E. planconiana | ARSEF 6252 | AF353723 | GQ285878 | – | – |
E. schizophorae | ARSEF 5348 | AF052402 | GQ285883 | – | – |
E. syrphi | ARSEF 5595 | – | DQ481230 | – | – |
E. tripidium | ARSEF 6518 | AF296755 | – | – | – |
Erynia conica | ARSEF 1439 | AF368513 | EF392396 | – | EF392506 |
E. ovispora | ARSEF 400 | JX242620 | JX242601 | – | JX242641 |
E. rhizospora | ARSEF 1441 | AF368514 | EF392397 | – | EF392507 |
E. sciarae | ARSEF 1870 | AF368515 | EF392399 | – | EF392509 |
Furia americana | ARSEF 742 | EF392554 | EF392389 | – | – |
F. gastropachae | ARSEF 5541 | EF392562 | EF392407 | – | EF392516 |
F. ithacensis | ARSEF 663 | EF392553 | EF392388 | – | EF392501 |
F. neopyralidarum | ARSEF 1145 | AF368518 | EF392394 | – | EF392504 |
F. pieris | ARSEF 781 | AF368519 | EF392390 | – | EF392502 |
F. virescens | ARSEF 1129 | EF392555 | EF392393 | – | EF392503 |
Gaertneriomyces semiglobiferus | AFTOL 34 | AF164247 | DQ273778 | DQ275338 | – |
Macrobiotophthora vermicola | ARSEF 650 | AF052400 | – | – | – |
Massospora cicadina | ARSEF 374 | EF392548 | EF392377 | – | EF392492 |
Mortierella verticillata | AFTOL 141 | AF157145 | DQ273794 | – | – |
Pandora blunckii | ARSEF 217 (T) | JX242621 | JX242602 | – | – |
P. delphacis | ARSEF 459 | AF368521 | EF392384 | – | EF392497 |
P. dipterigena | ARSEF 397 | AF368522 | EF392380 | – | EF392565 |
P. kondoiensis | CBS 642.92 | JX242622 | JX242603 | – | JX242642 |
P. neoaphidis | ARSEF 3240 | EF392560 | EF392405 | – | EF392514 |
Piptocephalis corymbifera | AFTOL 145 | AB016023 | AY546690 | DQ282619 | – |
Rhizophagus intraradices | AFTOL 845 | DQ322630 | FJ461839 | DQ282611 | – |
Rozella allomycis | AFTOL 297 | AY635838 | DQ273803 | DQ275342 | – |
Schizangiella serpentis | ARSEF 2237 | AF368523 | EF392428 | – | EF392488 |
Strongwellsea castrans | – | AF052406 | – | – | – |
Zancudomyces culisetae | AFTOL 29 | AF277007 | DQ273773 | – | – |
Zoophthora anglica | ARSEF 396 | – | EF392379 | – | EF392493 |
Z. lanceolata | ARSEF 469 | EF392550 | EF392385 | – | EF392498 |
Z. phalloides | ARSEF 2281 | EF392558 | EF392400 | – | EF392510 |
Z. radicans | ARSEF 388 | JX242624 | JX242605 | – | JX242644 |
More available nucLSU, nucSSU, mtSSU and EF-1α sequences of 14 Conidiobolus species and 47 other entomophthoroid fungi were obtained from GenBank. Ten species of Glomeromycotina, Mortierellomycotina, Mucoromycotina, Kickxellomycotina, Zoopagomycotina, Blastocladiomycota, Chytridiomycota and Cryptomycota, were chosen as outgroups. Alignments were constructed separately for each locus with MUSCLE 3.8.31 (
The combined dataset contained 4521 characters of nucLSU (1–1326), nucSSU (1327–3424), EF-1α (3425–4062) and mtSSU (4063–4521) after alignment. With the optimal model GTR+I+G and random starting trees, four Markov chains were run for 7 million generations and every 100th generation was sampled once. ML and BI analyses of the combined dataset resulted in phylogenetic reconstructions with almost similar topologies and the average standard deviation of split frequencies was 0.006721 (BI).
In the ML phylogenetic tree (Figure
Phylogenetic tree constructed by maximum likelihood analyses of nucLSU, nucSSU, EF-1α and mtSSU sequences for Entomophthoromycotina, with some chytrid and mucoralean fungi as outgroups. Three new genera and one Chinese new record are shown in red. Maximum likelihood bootstrap values (≥ 50%) / Bayesian posterior probabilities (≥ 0.50) of main clades are indicated along branches. Scale bar indicates substitutions per site.
In order to provide a more natural taxonomic classification, four genera (Capillidium, Conidiobolus, Microconidiobolus and Neoconidiobolus) and their type species (Ca. heterosporum, C. utriculosus, M. paulus and N. thromboides) are described here in this paper. Additionally, a new record Ca. adiaeretum, C. coronatus and C. iuxtagenitus with new isolates from China and C. khandalensis being first reported to produce microconidia are illustrated herein.
Referring to unique ellipsoidal secondary conidia (capilliconidia).
Capillidium heterosporum (Drechsler) B. Huang & Y. Nie.
Mycelia colourless. Primary conidiophores simple, bearing a single primary conidia. Primary conidia forcibly discharged multinucleate, colourless, globose, pyriform to obovoid. Two kinds of replicative conidia, the first one is similar and smaller than primary conidia, the second one (capilliconidia) arises from elongate and slender conidiophores. Zygospores present or absent, formed in axial alignment with conjugating segments, globose to subglobose, often smooth, sometimes rough, colourless or yellowish.
Conidiobolus subgen. Capillidium Ben-Ze’ev & Kenneth was firstly established to include species with capilliconidia (
Conidiobolus heterosporus Drechsler, Am. J. Bot. 40: 107 (1953). Basionym.
=Conidiobolus rugosus Drechsler, Am. J. Bot. 42: 437 (1955).
China, Anhui Province, Plant detritus, 8 Nov 2008, C.F. Wang,
Colonies on PDA at 25 °C after 3 d, white, reaching ca. 21 mm in diameter. Mycelia colourless, 5–9 μm wide. Primary conidiophores, colourless, unbranched and producing a single globose conidium with widening upwards, extending to a length of 30–245 μm into the air, 8–17 μm wide. Primary conidia forcibly discharged, colourless, globose to subglobose, measuring 12–37 μm in greatest length and 11–31 μm in total width, including a basal papilla 1.5–5 μm high and 5–12 μm wide. After discharging on to 2% water-agar, similar and smaller secondary conidia arise from primary conidia, 1–6 ellipsoidal secondary conidia (capilliconidia, 10–20 × 12–38 μm) arise from slender conidiophores (50–250 × 2.5–4 μm). Resting spores not observed.
The ex-type living culture is
Capillidium heterosporum a colony on PDA after 3 d at 25 °C b primary conidiophores bearing primary conidia c primary conidia d, e, f ellipsoidal secondary conidia arising from slender conidiophores g, h production of secondary conidia. Scale bars: 10 mm (a); 20 μm (b, c, d, g, h); 100 μm (e, f).
Conidiobolus adiaeretus Drechsler, J. Wash. Acad. Sci. 43: 42 (1953). Basionym.
China, Jiangsu Province, Nanjing City, Laoshan Forest Park, 32°5'58"N, 118°35'53"E, Plant detritus, 1 Dec 2018, Y. Nie and Y. Gao, HMAS 248358, culture
Colonies on PDA at 25 °C after 3 d, white, reaching ca. 7–10 mm in diameter. Mycelia colourless, 3–4.5 μm wide. Primary conidiophores, colourless, unbranched and producing a single globose conidium with widening upwards; they offer a pronounced dimensional contrast with the mycelial filaments, extending to a length of 50–210 μm into the air, 3–25 μm wide. Primary conidia forcibly discharged, colourless, globose, measuring 15–45 μm in greatest length and 13–42 μm in total width, including a basal papilla 2–6 μm high and 5–17 μm wide. After discharging on to 2% water-agar, similar and smaller secondary conidia arise from primary conidia, two generations of multiple spherical units forming on the parent globose conidia Microconidia only formed from the second set, 5–12 × 9–10 μm. Capilliconidia formed readily from discharged microconidia, 16–24 × 5–6 μm. Chlamydospores formed within the substratum, colourless, globose to ellipsoidal, 13–40 × 15–45 μm.
The species was firstly reported from America (
Capillidium adiaeretum a colony on PDA after 3 d at 25 °C b mycelia c, d primary conidiophores bearing primary conidia e, f primary conidia g Production of secondary conidia h first stage of forming microconidia i second stage of forming microconidia j, k ellipsoidal secondary conidia arising from slender conidiophores l chlamydospores. Scale bars: 10 mm (a); 100 μm (b); 20 μm (c–l).
= Delacroixia Sacc. & P. Syd., Syll. fung. (Abellini) 14(1): 457 (1899).
Conidiobolus subgen. Delacroixia (Sacc. & P. Syd.) Tyrrell & Macleod, J. Invert. Pathol. 20: 12 (1972).
Conidiobolus utriculosus Bref.
Mycelia colourless. Primary conidiophores simple or branched dichotomously, positively phototropic, bearing a single or 2–4 primary conidia. Primary conidia forcibly discharged, multinucleate, colourless, pyriform, obovoid, globose to subglobose. Secondary conidia usually with shape of primary conidia but smaller, formed singly on short secondary conidiophores. Microspores arising from primary or secondary conidia. Villose appendaged globose conidia and formed villose conidia. Chlamydospores formed intercalarily within assimilative hyphae. Zygospores formed in axial alignment with one or two (homothallic or heterothallic) conjugating segments.
C. utriculosus, the type species of the genus Conidiobolus, has not been re-collected since Brefeld isolated it in 1884 and most taxonomists working on entomophthoroid fungi now universally recognised it as C. coronatus (
= Conidiobolus minor Bref., Mykol. Untersuch. 6(2): 35, 68 (1884).
No ex-type.
Refer to
Due to the lack of ex-type, plates 3, 4, and 5 in Brefeld, Mykol. Untersuch. 6(2): 35 (1884) are designated here as the lectotype for Conidiobolus utriculosus.
Boudierella coronata Costantin, Bull. Soc. mycol. Fr. 13: 40 (1897). Basionym.
Delacroixia coronata (Costantin) Sacc. & P. Syd., Syll. fung. (Abellini) 14(1): 457 (1899).
Entomophthora coronata (Costantin) Kevorkian, J. Agric. Univ. Puerto Rico 21(2): 191 (1937).
= Conidiobolus villosus G.W. Martin, Bot. Gaz. 80(3): 317 (1925).
China, Shandong Province, Plant detritus, 20 Mar 2009, C.F. Wang,
Colonies grown on PDA for 3 d at 21 °C, reaching ca. 65 mm in diameter. Mycelia colourless, 8–20 μm wide. Primary conidiophores, positively phototropic, colourless, unbranched and producing a single globose conidium, extending to a length of 53–287 μm into the air, 7.5–20.5 μm wide. Primary conidia forcibly discharged, colourless, globose, measuring 36–52 μm in greatest width and 42–65 μm in total length, including a basal papilla 12–18 μm high and 6.5–14 μm wide. After discharging on to 2% water-agar, similar and smaller secondary conidia arise from primary conidia. Microconidia produced readily from primary conidia, globose or almond-shaped, 13–19 × 11–15 μm. Villose spores formed after 4–5 d, globose, 20–42 μm.
The ex-type living culture is
China, Anhui Province, Plant detritus, 8 Nov 2008, C.F. Wang,
Colonies on PDA at 21 °C after 3 d white, flat, slow-growing, reaching ca. 13 mm in diameter. Mycelia colourless, 5.5–11 μm wide. Primary conidiophores, positively phototropic, arising from hyphal segments, colourless, 28–75 × 7.5–10 μm, unbranched and producing a single globose conidium. Primary conidia forcibly discharged, globose, 27–37 × 21–28 μm, with a basal papilla 6–10 μm wide. Secondary conidia arising from primary conidia, similar to, but smaller than the primary ones, forcibly discharged. Tertiary conidium fusiform arising from primary conidia, 30–45 × 16–22 μm. Zygospores in a position separated by a short beak near a lateral conjugation, globose to subglobose, smooth, 21–25 × 17–24 μm, with a 1–2 μm thick wall.
The ex-type living culture is ARSEF 6378 (United Kingdom, Staffordshire, Plant detritus, 31 October 1983, M. F. Smith).
a–g Conidiobolus iuxtagenitus h Conidiobolus khandalensis a colony on PDA after 3 d at 21 °C b primary conidiophores bearing primary conidia c primary conidia d tertiary fusiform conidium from a globose spore e zygospore formation with the beak almost emptied of protoplasm f production of secondary conidia g zygospores h microconidia produced from global conidia. Scale bars: 10 mm (a); 20 μm (b–h).
India, Khandala, Dec. 1961, Srinivasan and Thirumalachar,
Refer to
According to the original morphological description (
Referring to small discharged primary conidia.
Microconidiobolus paulus (Drechsler) B. Huang & Y. Nie.
Mycelia colourless. Primary conidiophores simple and short, bearing a single primary conidia. Primary conidia forcibly discharged, multinucleate, colourless, globose to obovoid, usually small, mostly less than 20 μm. Only globose replicative conidia produced, similar and smaller than primary conidia. Chlamydospores globose, formed terminally on hyphae or from globose cells by thickening of the wall. Zygospores formed in axial alignment with two conjugating segments, globose to ellipsoidal, smooth and yellowish.
This genus includes three species producing smaller primary conidia (mostly less than 20 μm) without microspores or capilliconidia compared to other Conidiobolus spp. These three species are C. nodosus, C. paulus and C. terrestris. According to the taxonomic scheme of Conidiobolus by
Conidiobolus paulus Drechsler, Bull. Torrey bot. Club. 84: 269 (1957). Basionym.
= Conidiobolus undulatus Drechsler, Bull. Torrey bot. Club. 84: 275 (1957).
= Conidiobolus parvus Drechsler, Bull. Torrey bot. Club. 89: 233 (1962).
Refer to
The ex-type living culture is
Referring to the subgenus Conidiobolus raised to generic rank.
Neoconidiobolus thromboides (Drechsler) B. Huang & Y. Nie.
Mycelia colourless. Primary conidiophores simple, sometimes branched from hyphal knots or differentiated from aerial hyphae, positively phototropic, bearing a single primary conidium. Primary conidia forcibly discharged, multinucleate, colourless, globose, pyriform to obovoid. Replicative conidia similar and smaller than primary conidia. Chlamydospores globose, formed terminally on hyphae or from globose cells by thickening of the wall. Zygospores formed in axial alignment with two conjugating segments, globose to ellipsoidal, smooth, colourless, rarely pale yellowish.
The genus Neoconidiobolus is strikingly similar to the subgenus Conidiobolus which produces neither microconidia nor capilliconidia. All members in the clade of Neoconidiobolus share the following characteristics: forcibly discharged, colourless, globose, pyriform to obovoid primary conidia. Two kinds of replicative conidia produced. One is discharged, similar and smaller than primary conidia and the other is elongate and forcibly discharged. Two types of resting spores produced: zygospores and chlamydospores.
Conidiobolus thromboides Drechsler, J. Wash. Acad. Sci. 43: 38 (1953). Basionym.
China, Anhui Province, Plant detritus, 21 Feb 2009, C.F. Wang,
Colonies grown on PDA for 3 d at 25 °C, white, reaching ca. 30 mm diameter. Mycelium colourless, filamentous, 5–7.5 µm wide. Primary conidiophores colourless, unbranched and producing a single conidium, 50–122.5 × 6–16.5 µm. Primary conidia forcibly discharged, colourless, globose to subglobose, 20–26.5 µm wide, 26.5–34 µm long, including a basal papilla 6–10 µm wide. Secondary conidia globose, forming from the primary conidia. Zygospores most often formed between segments of separate hyphae. Mature zygospores smooth, globose to subglobose, 25–30 μm in diameter with wall 2–3 μm thick.
The ex-type living culture is
In addition to previously described taxa, more new combinations were proposed herein and their descriptions refer to relevant protologues.
Conidiobolus bangalorensis Sriniv. & Thirum., Mycologia 59(4): 702 (1967). Basionym.
Conidiobolus denaeosporus Drechsler, J. Wash. Acad. Sci. 47: 309 (1957). Basionym.
Conidiobolus lobatus Sriniv. & Thirum., J. Elisha Mitchell scient. Soc. 84: 212 (1968). Basionym.
Conidiobolus pumilus Drechsler, J. Wash. Acad. Sci. 45: 115 (1955). Basionym.
= Conidiobolus globuliferus Drechsler, Am. J. Bot. 43: 783 (1957) [1956].
= Conidiobolus inordinatus Drechsler, J. Wash. Acad. Sci. 47: 312 (1957).
Conidiobolus rhysosporus Drechsler, Am. J. Bot. 41: 567 (1954). Basionym.
Conidiobolus nodosus Sriniv. & Thirum., Mycologia 59(4): 705 (1967). Basionym.
Conidiobolus terrestris Sriniv. & Thirum., Mycopathol. Mycol. appl. 36(3–4): 344 (1968). Basionym.
Conidiobolus couchii Sriniv. & Thirum., J. Elisha Mitchell scient. Soc. 84: 211 (1968). Basionym.
Conidiobolus lachnodes Drechsler, Am. J. Bot. 42: 442 (1955). Basionym.
Conidiobolus mirabilis Y. Nie & B. Huang, Mycol. Progr. 17(10): 1204 (2018). Basionym.
Conidiobolus osmodes Drechsler, Am. J. Bot. 41: 571 (1954). Basionym.
= Conidiobolus antarcticus S. Tosi, Caretta & Humber, Mycotaxon 90(2): 344 (2004).
Conidiobolus pachyzygosporus Y. Nie & B. Huang, Mycol. Progr. 17(10): 1206 (2018). Basionym.
Conidiobolus sinensis Y. Nie, X.Y. Liu & B. Huang, Mycotaxon 120: 432 (2012). Basionym.
Conidiobolus stilbeus Y. Nie & B. Huang, Mycosphere 7(6): 804 (2016). Basionym.
Conidiobolus stromoideus Sriniv. & Thirum., Sydowia 16(1–6): 65 (1963) [1962]. Basionym.
Entomophthora vermicola J.S. McCulloch, Trans. Br. mycol. Soc. 68(2): 173 (1977). Basionym.
Macrobiotophthora vermicola (J.S. McCulloch) B.E. Tucker, Mycotaxon 13(3): 499 (1981).
The phylogenetic position of Basidiobolus in the Kingdom Fungi has been problematic for a long time. Previous phylogenetic analyses of the rDNA (18S, 28S and 5.8S) sequences grouped Basidiobolus outside or basal in the Entomophthorales (
The phylogenetic relationship of the genus Conidiobolus has been unclear for a long time, because of its high heterology (
In Clade I of the genus Capillidium, seven species grouped in a monophyletic clade with good support (100/1.00) and the synapomorph of producing capilliconidia: Conidiobolus adiaeretus (= Capillidium adiaeretum), Co. bangalorensis (= Ca. bangalorensis), Co. denaeosporus (= Ca. denaeosporum), Co. heterosporus (= Ca. heterosprum), Co. lobatus (= Ca. lobatum), Co. pumilus (= Ca. pumilum) and Co. rhysosporus (= Ca. rhysosporum). As a note, Co. denaeosporus was synonymised with Co. pumilus (
In Clade II of the genus Neoconidiobolus, all 14 strains comprising 10 species produce neither microspores nor capilliconidia. Amongst these, C. antarcticus was identified as a synonym of C. osmodes (
Considering its long history and significant impact, we kept and emended the genus Conidiobolus and the original illustrations of the type species C. utriculosus (
In Clade IV of the genus Microconidiobolus, Conidiobolus undulatus was identified as a synonym of C. paulus (= M. paulus) by
Phylogenetically, Conidiobolus lamprauges does group with Clade III and received strong bootstrap support (100/1.00). Morphologically, this species produces small primary conidia (12.5–20 × 15–22 μm) without microconidia or capilliconidia and is similar to species within Clade IV. Its taxonomic status remains unclear in the present study.
We thank Dr. Z.F. Yu (Yunnan University) for improving the manuscript. We also thank Y. Gao (Jiangxi Agricultural University) for collecting some Conidiobolus strains. This project was supported by the National Natural Science Foundation of China (Nos. 31900008, 30770008 and 31670019).