Yeast microbiota of free-ranging amphibians and reptiles from Caatinga biome in Ceará State, Northeast Brazil: High pathogenic potential of <i>Candida famata</i>

Castelo-Branco, Débora de Souza Collares Maia; Graça-Filho, Renan Vasconcelos da; Oliveira, Jonathas Sales de; Rocha, Maria Gleiciane da; Araújo, Géssica dos Santos; Araújo Neto, Manoel Paiva de; Cordeiro, Rossana de Aguiar; Pereira-Neto, Waldemiro de Aquino; Sidrim, José Júlio Costa; Brilhante, Raimunda Sâmia Nogueira; Rocha, Marcos Fábio Gadelha

doi:10.1590/0103-8478cr20200742

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MICROBIOLOGY • Cienc. Rural 51 (7) • 2021 • https://doi.org/10.1590/0103-8478cr20200742 linkcopy

Yeast microbiota of free-ranging amphibians and reptiles from Caatinga biome in Ceará State, Northeast Brazil: High pathogenic potential of Candida famata

Leveduras da microbiota de anfíbios e répteis do bioma Caatinga no Ceará, Nordeste do Brasil: alto potencial patogênico de Candida famata

Authorship SCIMAGO INSTITUTIONS RANKINGS

Studies on the fungal microbiota of reptiles and amphibians are necessary to better understand of host-microbe interactions and the establishment of fungal disease in these animals. However, these studies are limited. The present researchidentified yeasts from free-ranging reptiles and amphibians from the Caatinga biome andevaluated the virulence factors production, the antifungal susceptibility in planktonic and biofilm growth and the pathogenicity of Candida famata isolates. Twenty-nine isolates of the genera Candida, Cryptococcus and Rhodotorula were identified by phenotypic and/or molecular methods and production of hydrolytic enzymes in vitro by these genera of fungi was evaluated. In addition, susceptibility of planktonic cells and biofilms to azoles and amphotericin B was evaluated. The pathogenicity of C. famata, the most prevalent yeast species isolated, was evaluated using Caenorhabditis elegans model. C. famata was the most prevalent yeast in amphibian and reptilian microbiota. Phospholipase and protease production was observed in 18/29 and 11/29 of the yeast isolates, respectively, while 100% formed biofilms. Itraconazole presented high minimal inhibitory concentrations against C. famata and C. tropicalis. Amphotericin B reduced the biomass and metabolic activity of biofilms. C. famata induced the mortality of C. elegans. In conclusion, reptiles and amphibians are colonized by yeasts capable of producing important virulence factors, especially by Candida spp. that present low susceptibility to azoles which may result from imbalances in ecosystem. Finally, C. famata isolated from these animals presented high pathogenicity, showing the importance of the study of reptile and amphibians fungal microbiota.

Key words:
herpetofauna; yeasts; antifungal; virulence; pathogenicity

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Universidade Federal de Santa Maria Universidade Federal de Santa Maria, Centro de Ciências Rurais , 97105-900 Santa Maria RS Brazil , Tel.: +55 55 3220-8698 , Fax: +55 55 3220-8695 - Santa Maria - RS - Brazil
E-mail: cienciarural@mail.ufsm.br

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[TFN1] AMB: amphotericin B; FLC: fluconazole; ITC: itraconazole; VRC: voriconazole. ^aindicates the number of isolates. PHz and PRz: indicate the production of phospholipase and protease, respectively, based on the ratio between the size of the yeast colony and the total diameter (colony and halo). When PHz=1 and PRz=1, the isolate is negative for exoenzyme production. ^*Resistance.

Animal Species	Anatomical site	Yeast species	Minimum Inhibitory Concentration - MIC (µg/mL)			Exoenzymes
			AMB	FLC	ITC	VRC	PHz	PRz
--------------------------------------Snakes-----------------------------------
Lygophis dilepis	Oral cavity	Candida famata (1)^a	0.06	2	4^*	0.125	0.79	1
Lygophis dilepis	Oral cavity	Rhodotorula rubra (1)	0.5	<0.125	0.5	8	1	1
Boa constrictor	Oral cavity	Candida tropicalis (1)	0.06	4	16^*	0.06	0.89	1
Boa constrictor	Cloaca	C. tropicalis (1)	0.06	1	0.25	0.06	1	0.79
Micrurus ibiboboca	Oral Cavity	C. tropicalis (1)	0.06	1	0.06	0.06	0.76	0.95
	Cloaca	C. tropicalis (1)	0.06	1	0.06	0.06	0.91	0.68
	Cloaca	Cryptococcus neoformans (1)	2	4	0.06	0.125	0.85	1
Psomorphis jeobestis	Oral cavity	Candida metapsilosis (1)	0.06	0.5	0.03	0.03	0.88	1
Psomorphis jeobestis	Oral cavity	C. famata (1)	0.03	0.5	0.03	0.03	0.64	1
-------------------------------------Lizards------------------------------------
Iguana iguana	Oral Cavity	Candida parapsilosis sensu stricto (1)	0.125	0.5	0.03	0.03	0.75	0.67
Iguana iguana	Cloaca	C. famata (1)	0.03	4	0.0625	<0.03	0.68	1
Tropidurus hispidus	Cloaca	C. neoformans (1)	0.5	4	0.03	0.03	0.88	1
--------------------------------------Frogs-------------------------------------
Leptodactylus sp.	Skin	C. parapsilosis s. s. (1)	0.03	4	0.06	0.03	1	0.8
Leptodactylus latrans	Cloaca	C. famata (3)	0.125	1	0.03 - 0.125	0.03 - 0.06	0.86 (1) 1 (2)	0.59 (1) 1 (2)
Leptodactylus latrans	Cloaca	C. tropicalis (1)	0.25	1	0.5	0.03	1	1
Leptodactylus vastus	Cloaca	C. tropicalis (1)	0.25	0.5	16^*	0.03	0.37	0.86
Pithecopus nordestinus	Oral cavity	C. famata (1)	0.03	4	0.06	0.125	1	1
--------------------------------------Toads------------------------------------
Rhinella granulosa	Skin	C. tropicalis (1)	0.25	2	2^*	1	0.6	0.81
Rhinella jimi	Oral cavity	C. famata (1)	0.03	1	0.03	0.03	1	0.84
	Oral cavity	C. parapsilosis s. s. (1)	0.25	1	<0.03	<0.03	1	0.75
	Skin	C. famata (5)	0.06 - 2	0.5 - 2	≤0.03 - 2^*	≤0.03 - 0.5	0.5-0.97 (4) 1 (1)	0.78 (1) 1 (4)
		Candida guilliermondii (1)	0.125	1	0.06	0.03	1	1
		R. rubra (1)	<0.03	2	1	1	0.72	1