First occurrence of Backusella gigacellularis (Mucorales, Mucoromycota) in a fragment of an Upland Forest within the semi-arid region of northeastern Brazil

Ana Lúcia Sabino de Melo Alves Leslie Warren Silva de Freitas Luciana Melo Sartori Gurgel Joana D’Arc Alves Leitão Thalline Rafhaella Leite Cordeiro André Luiz Cabral Monteiro de Azevedo Santiago About the authors

Abstract

In a survey mucoralean fungi in the Brejo da Serra do Benedito, a fragment of Upland Forest in the semi-arid region of Pernambuco, Brazil, a specimen of Backusella gigacellularis was isolated. So far, B. gigacellularis (holotype) had only been isolated from soil in the Cerrado domain, in São Paulo state, southeastern Brazil. This is the second report of B. gigacellularis worldwide, and the first record to northeastern Brazil. A detailed description, as well as the illustration of the specimen, are presented.

Key words:
Mucoromyceta; soil; taxonomy; zygosporic fungi

Resumo

Em um levantamento de espécies de fungos Mucorales no Brejo da Serra do Benedito, um Brejo de altitude do semi-árido pernambucano, Brasil, um espécime de Backusella gigacellularis foi isolado. Até o momento, B. gigacellularis (holótipo) só havia sido isolada de solo no Domínio Cerrado, no estado de São Paulo, sudeste do Brasil. Este é segundo registro mundial de B. gigacellularis e o primeiro para o nordeste do Brasil, especificamente em um a área de Brejo de altitude. Nesse trabalho, são apresentadas uma descrição detalhada e ilustração do espécime isolado.

Palavras-chave:
Mucoromycota; solo; taxonomia; Fungos zigospóricos

The Brazilian semi-arid region, characterized by high average temperatures, scarce precipitation, and soil with low productivity potential (Giulietti et al. 2006Giulietti AM, Conceicao A & Queiroz LP (2006) Diversidade e caracterização das fanerógamas do semi-árido brasileiro. Associacão Plantas do Nordeste, Recife. 488p.), predominantly supports typical vegetation of the caatinga domain, which tolerates and is adapted to semi-arid climatic conditions. The Upland Forest areas are enclaves of humidForest surrounded by vegetation of Caatinga, forming “islands” of rainforest in the middle of the semi-arid region that present different climatic conditions in relation to humidity, temperature and vegetation in comparison with areas of Caatinga (Tabarelli & Santos 2004Tabarelli M & Santos AMM (2004) Uma breve descrição sobre a história natural dos Brejos nordestinos. In: Porto KC, Cabral JJP & Tabarelli M (eds.) Brejos de altitude em Pernambuco e Paraíba - História Natural, Ecologia e Conservação. Ministério do Meio Ambiente, Brasilia. Pp. 17-24.).

Considering the elevated diversity and endemism of plants in the Atlantic Forest domain, it is probable that the current knowledge of diversity of mucoralean species in soils of the Upland Forest areas is insufficient (Lima et al. 2018aLima DX, Cordeiro TFL, Souza CAF, Santiago ALCMA & Souza-Motta CM (2018a) Diversity of basal fungal order Mucorales (Mucoromycota) in a remaining area of the Brazilian Atlantic Rainforest. Nova Hedwigia 107: 459-471.). So far, 34 species of Mucorales have been reported for the Brazilian Upland Forest areas, including six recently described new species (Hyde et al. 2016Hyde KD, Hongsanan S, Jeewon R, Bhat JD, McKenzie EH, Jones EBG, Phookamsa R, Ariyawansa AH, Boonmee S, Zhao Q, Abdel-Aziz FA, Abdel-Waha MA, Banmai S, Chomnunti P, Cui B, Daranagama DA, Das K, Dayarathn MC, Silva NI, Dissanayake AJ, Doilom M, Ekanayaka AH, Gibertoni TB, Go’es-Neto A, Huang S, Jayasiri SC, Jayawardena RS, Konta S, Lee HB, Li W, Lin C, Liu J, Lu Y, Luo Z, Manawasinghe IS, Manimohan P, Mapook A, Niskanen T, Norphanphoun C, Papizadeh M, Perera RH, Phukhamsakda C, Richter CC, Santiago ALCMA, Drechsler-Santos ER, Senanayake IC & Tanaka K (2016) Fungal diversity notes 367-490: taxonomic and phylogenetic contributions to fungal taxa. Fungal Diversity 80: 1-270.; Tibpromma et al. 2017Tibpromma S, Hyde KD, Jeewon R, Maharachchikumbura SSN, Liu JK, Bhat DJ, Jones EBG, McKenzie EHC, Camporesi E, Tibpromma TS, Jeewon R, Bulgakov TS, Doilom M, Santiago ALCMA, Das K, Manimohan P, Gibertoni TB, Lim YW, Ekanayaka AH, Thongbai B, Lee HB, Yang JB, Kirk PM, Sysouphanthong P, Singh SK, Boonmee S, Dong W, Anil Raj KN, Latha KPD, Phookamsak R, Phukhamsakda C, Konta S, Jayasiri SC, Norphanphoun C, Tennakoon DS, Li J, Dayarathne MC, Perera RH, Xiao Y, Wanasinghe DN, Senanayake IC, Goonasekara ID, Silva NI, Mapook A, Jayawardena RS, Dissanayake AJ, Manawasinghe IS, Chethana KWT, Luo ZL, Hapuarachchi KK, Baghela A, Soares AM, Vizzini A, Meiras-Ottoni A, Mešić A, Dutta AK, Souza CAF, Richter C, Lin CG, Chakrabarty D, Daranagama DA, Lima DX, Chakraborty D, Ercole E, Wu F, Simonini G, Vasquez G, da Silva GA, Plautz Jr. HL, Ariyawansa HA, Lee H, 30, Kušan I, Song J, Sun J, Karmakar J, Hu K, Semwal KC, Thambugala KM, Voigt K, Acharya K, Rajeshkumar KC, Ryvarden L, Jadan M, Hosen MI, Mikšík M, Samarakoon MC, Wijayawardene NN, Kim NK, Matočec N, Singh PN, Tian Q, Bhatt RP, de Oliveira RJV, Tulloss RE, Aamir S, Kaewchai S, Marathe SD, Khan S, Hongsanan S, Adhikari S, Mehmood T, Bandyopadhyay TK, Svetasheva TY, Nguyen TTT, Vladimır A, Li W-J, Wang Y, Indoliya Y, Tkalčec Z, Elgorban AM, Bahkali AH, Tang AMC, Su H-Y, Zhang H, Promputtha I, Luangsa-ard J, Xu J, Yan J, Ji-Chuan K, Stadler M, Mortimer PE, Chomnunti P, Zhao Q, Phillips AJL, Nontachaiyapoom S, Wen T-C, Karunarathna SC (2017) Fungal diversity notes 491-602: taxonomic and phylogenetic contributions to fungal taxa. Fungal Diversity 83: 1-261.; Lima et al. 2018bLima CLF, Lima DX, Souza CAF, Oliveira RJV, Cavalcanti IB, Gurgel LMS & Santiago ALCMA (2018b) Description of Mucor pernambucoensis (Mucorales, Mucoromycota), a new species isolated from the Brazilian Upland Rainforest. Phytotaxa 350: 274-282.) and two first occurrences for Brazil (Santiago & Maia 2010Santiago ALCMA & Maia LC (2010) Two new records of Mucorales from the Brazilian semi-arid region. Mycotaxon 114: 17-20.; Alves et al. 2017Alves ALSM, Souza CAF, Oliveira RJV, Cordeiro TRL & Santiago ALCMA (2017) Cunninghamella clavata from Brazil: a new record for the western hemisphere. Mycotaxon 132: 381­­­-389.).

The genus Backusella, described by Ellis & Hesseltine (1969Ellis JJ & Hesseltine LW (1969) A new member of the Mucorales. Mycologia 61: 863­­­-872.), was created to accommodate species that produce terminal multispored sporangia as well as uni- and/or multispored sporangiola that arise laterally from sporangiophores (Benny 2005Benny GL (2005) Zygomycetes. Available at <http://www.zygomycetes.org>. Access on 24 May 2019.
http://www.zygomycetes.org...
). Backusella specimens are commonly isolated from soil and rodent dung (Benny & Benjamin (1975)Benny GL & Benjamin RK (1975) Observations on Thamnidiaceae (Mucorales). New taxa, new combinations, and notes on selected species. Aliso 8: 301-351.. This genus underwent modifications by Benny & Benjamin (1975)Benny GL & Benjamin RK (1975) Observations on Thamnidiaceae (Mucorales). New taxa, new combinations, and notes on selected species. Aliso 8: 301-351., who have proposed B. lamprospora (≡ Mucor lamprosporus Lendn.) and B. ctenidia (≡ Thamnidium ctenidium Durrell & M. fkeming). Walther et al. (2013Walther G, Pawłowska J, Alastruey-Izquierdo A, Wrzosek M, Rodriguez-Tudela JL, Dolatabadi S, Chakrabarti A & Hoog GS (2013) DNA barcoding in Mucorales: an inventory of biodiversity. Persoonia 30: 11-47.), in a review using ITS and LSU sequences of rDNA, proposed more significant changes, with the transference of all species of Mucor Fresen. with transiently recurved sporangiophores when young to Backusella. Currently, this genus comprises fifteen species: B. azygospora T.R.L. Cordeiro, Hyang B. Lee & A.L. Santiago, B. constricta D.X. Lima, C.A.F. de Souza & A.L. Santiago, B. circina J.J. Ellis & Hesselt., B. gigacellularis J.I. de Souza, Pires-Zottarelli & Harakava, B. grandis (Schipper & Samson) Walther & de Hoog, B. granulispora L.S. Loh & Kuthub, B. indica (Baijal & B.S. Mehrotra) Walther & de Hoog, B. johorensis L.S. Loh, Nawawi & Kuthub, B. lamprospora (Lendn.) Benny & R.K. Benj., B. locustae Hyang B. Lee, S.H. Lee & T.T.T Nguyen, B. oblongielliptica(H. Nagan., Hirahara & Seshita ex Pidopl. & Milko) Walther & de Hoog,B. oblongispora (Naumov) Walther & de Hoog, B. recurva (E.E. Butler) Walther & de Hoog, B. tuberculispora (Schipper) Walther & de Hoog, B. variabilis (A.K. Sarbhoy) Walther & de Hoog. For Brazil, B. azygospora, B. lamprospora, B. gigacellularis and B. constricta have been recorded.

During a survey of Mucorales species in soils of an Upland Forest area located in the semiarid region of Pernambuco, B. gigacellularis was isolated and is being reported for the first time from northeastern Brazil. This species had previously only been isolated in the Cerrado biome in São Paulo state, Brazil (de Souza et al. 2014De Souza JI, Marano AV, Pires-Zottarelli CLA, Chambergo FS & Harakava R (2014). A new species of Backusella (Mucorales) from a Cerrado reserve in Southeast Brazil. Mycological progress 13: 975-980.).

For isolation, five milligrams of soil were added to wheat germ agar culture medium (Benny 2008Benny GL (2008) The methods used by Dr. R.K. Benjamin, and other mycologists to isolate Zygomycetes. Aliso 26: 37-61.) amended with chloramphenicol (80 mg.L-1) in Petri dishes in triplicate. The growth of colonies was monitored for 96 hours at room temperature (28 ± 2 °C). In order to purify the Mucorales, fragments of the colonies were transferred separately to MEA (malt extract agar medium) (Benny 2008Benny GL (2008) The methods used by Dr. R.K. Benjamin, and other mycologists to isolate Zygomycetes. Aliso 26: 37-61.) plus chloramphenicol (80 mg.L-1). The specimen was identified through observation of macroscopic (color, appearance, and diameter of the colony) and microscopic (shape and size of sporangiophores, columellae, sporangia, sporangiospores, and giant cells) characteristics based on the description of de Souza et al. (2014)De Souza JI, Marano AV, Pires-Zottarelli CLA, Chambergo FS & Harakava R (2014). A new species of Backusella (Mucorales) from a Cerrado reserve in Southeast Brazil. Mycological progress 13: 975-980..

Backusella gigacellularis J.I. de Souza, Pires-Zottarelli & Harakava, Mycol. Progr. 13: 976 (2015). Fig. 1

Figure 1
a-e. Backusella gigacellularis (URM 7894) - a. unbranched sporangiophore with sporangium; b. unbranched sporangiophore with columella; c. sympodially branched sporophore bearing only sporangiola; d. sporangiospores; e. giant cell. Bars: a, b, c, d, e = 25 µm.

Colony white-yellowish, reverse yellow, colonizing the entire Petri dish (9 cm diam. and 1.5 cm high) in 5 days, at 25 °C, in MEA. Sporangiophores hyaline, some with greenish-brown contents, arising from the substrate, recurved when young and becoming erect when mature, up to 20 µm in diam, monopodially branched, mostly with short branches and slightly encrusted wall. Sporangia globose, with smooth and deliquescent wall, up to 130 µm in diam. Columellae globose, subglobose, conical and slightly cylindrical, 20-40 (-50) × 20-45 µm, hyaline, with slightly encrusted wall, some with brown contents; collar commonly present with needle-shaped spines. Multispored sporangiola arising from pedicels, hyaline, with equinulated wall, globose to subglobose 9.5­-28 µm in diam. Unispored sporangiola absent. Columellae of sporangiola conical and occasionally globose, hyaline, 7-12(-14) × 15-30 µm. Sporangiospores hyaline, smooth-walled, ellipsoid, irregular, a few subglobose (9-)16-33(-45) × (7-)9-17(-20) µm, with oil droplets. Giant cells, globose. Zygospores not observed.

Material examined: BRAZIL. Pernambuco: Gravatá, Serra do Benedito (08°17’58’’S, 35°35’29’’W), soil, A.L.S.M. Alves (URM 7894).

The species occurs in São Paulo and Pernambuco states, Brazil. This is the second report worldwide and the first report of this species in northeastern Brazil.

Minor morphological differences were observed between B. gigacellularis URM 7894 and the holotype described by de Souza et al. (2014)De Souza JI, Marano AV, Pires-Zottarelli CLA, Chambergo FS & Harakava R (2014). A new species of Backusella (Mucorales) from a Cerrado reserve in Southeast Brazil. Mycological progress 13: 975-980.. Sporangiophores up to 20 µm diam. were found in B. gigacellularis URM 7894, slightly larger than those described by de Souza et al. (2014)De Souza JI, Marano AV, Pires-Zottarelli CLA, Chambergo FS & Harakava R (2014). A new species of Backusella (Mucorales) from a Cerrado reserve in Southeast Brazil. Mycological progress 13: 975-980., which are up to 16.8 µm. We also observed globose, subglobose, conical and slightly cylindrical columellae, 20-40(-50) × 20-45 µm, whereas de Souza et al. (2014)De Souza JI, Marano AV, Pires-Zottarelli CLA, Chambergo FS & Harakava R (2014). A new species of Backusella (Mucorales) from a Cerrado reserve in Southeast Brazil. Mycological progress 13: 975-980. reported ellipsoid, cylindrical and rarely pyriform columellae, 9.4-53 × 8.2-46 µm. Sporangiola of B. gigacellularis URM 7894 were larger (up to 28 µm in diam) than the holotype sporangiola that were up to 23 µm in diam.

This work increases the knowledge of the Backusella genus in Brazil, especially in Upland Forest areas that are being severely degraded by anthropic influences.

Acknowledgemets

This manuscript was financed by the Project “Diversity of Mucoromycotina in the different ecosystems of the Atlantic Rainforest of Pernambuco” (FACEPE - First Projects Program PPP/FACEPE/CNPq - APQ - 0842-2.12/14). The authors also thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico, for the scholarship awarded to André L.C.M.A. Santiago, and the Coordenacão de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), for the scholarships provided to Ana L.S.M. Alves, Thalline R.L. Cordeiro, Joana D’Árc A. Leitão, and Leslie W.S. de Freitas.

References

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    » http://www.zygomycetes.org
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  • Benny GL & Benjamin RK (1975) Observations on Thamnidiaceae (Mucorales). New taxa, new combinations, and notes on selected species. Aliso 8: 301-351.
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  • Lima CLF, Lima DX, Souza CAF, Oliveira RJV, Cavalcanti IB, Gurgel LMS & Santiago ALCMA (2018b) Description of Mucor pernambucoensis (Mucorales, Mucoromycota), a new species isolated from the Brazilian Upland Rainforest. Phytotaxa 350: 274-282.
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  • Walther G, Pawłowska J, Alastruey-Izquierdo A, Wrzosek M, Rodriguez-Tudela JL, Dolatabadi S, Chakrabarti A & Hoog GS (2013) DNA barcoding in Mucorales: an inventory of biodiversity. Persoonia 30: 11-47.

Publication Dates

  • Publication in this collection
    18 Jan 2021
  • Date of issue
    2021

History

  • Received
    12 July 2019
  • Accepted
    27 Sept 2019
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