Description of new species of Mycobacterium terrae complex isolated from sewage at the São Paulo zoological park foundation in Brazil

Camila Lopes Romagnoli; Emilyn Costa Conceição; Edson Machado; Leonardo Bruno Paz Ferreira Barreto; Abhinav Sharma; Natalia Maria Silva; Lucas Evangelista Marques; Maria Aparecida Juliano; Maria Cristina da Silva Lourenço; Luciano Antonio Digiampietri; Philip Noel Suffys; Sylvia Cardoso Leão; Cristina Viana-Niero

doi:10.3389/fmicb.2024.1335985

Description of new species of Mycobacterium terrae complex isolated from sewage at the São Paulo zoological park foundation in Brazil

Front Microbiol. 2024 Jan 23:15:1335985. doi: 10.3389/fmicb.2024.1335985. eCollection 2024.

Authors

Affiliations

¹ Departamento de Microbiologia, Imunologia e Parasitologia, Universidade Federal de São Paulo, São Paulo, Brazil.
² Laboratório de Bacteriologia e Bioensaios em Micobactérias, Instituto Nacional de Infectologia Evandro Chagas, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil.
³ DSI-NRF Centre of Excellence for Biomedical Tuberculosis Research, SAMRC Centre for Tuberculosis Research, Division of Molecular Biology and Human Genetics, Faculty of Medicine and Health Sciences, Stellenbosch University, Cape Town, South Africa.
⁴ Laboratório de Biologia Molecular Aplicada a Micobactérias, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil.
⁵ Departamento de Biofísica, Universidade Federal de São Paulo, São Paulo, Brazil.
⁶ Escola de Artes, Ciências e Humanidades, Universidade Federal de São Paulo, São Paulo, Brazil.

Abstract

Five mycobacterial isolates from sewage were classified as members of the genus Mycobacterium but presented inconclusive species assignments. Thus, the isolates (MYC017, MYC098, MYC101, MYC123 and MYC340) were analyzed by phenotypical, biochemical, matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF-MS) and genomic features to clarify their taxonomic position. Phenotypic analysis and biochemical tests did not distinguish these isolates from other non-pigmented mycobacteria. In contrast, MALDI-TOF MS analysis showed that isolates were not related to any previously described Mycobacterium species. Comparative genomic analysis showed values of ANI and dDDH between 81.59-85.56% and 24.4-28.8%, respectively, when compared to the genomes of species of this genus. In addition, two (MYC101 and MYC123) presented indistinguishable protein spectra from each other and values of ANI = 98.57% and dDDH = 97.3%, therefore being considered as belonging to the same species. Phylogenetic analysis grouped the five isolates within the Mycobacterium terrae complex (MTC) but in a specific subclade and separated from the species already described and supported by 100% bootstrap value, confirming that they are part of this complex but different from earlier described species. According to these data, we propose the description of four new species belonging to the Mycobacterium genus: (i) Mycobacterium defluvii sp. nov. strain MYC017^T (= ATCC TSD-296^T = JCM 35364^T), (ii) Mycobacterium crassicus sp. nov. strain MYC098^T (= ATCC TSD-297^T = JCM 35365T), (iii) Mycobacterium zoologicum sp. nov. strain MYC101^T (= ATCC TSD-298^T = JCM 35366^T) and MYC123 (= ATCC BAA-3216 = JCM 35367); and (iv) Mycobacterium nativiensis sp. nov. strain MYC340^T (= ATCC TSD-299^T = JCM 35368^T).

Keywords: Brazil; MALDI-TOF-MS; Mycobacterium terrae complex; Mycolicibacter; non-tuberculous mycobacteria; taxonomy; whole-genome sequencing.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was provided by research grants 2019/14137-4 from Fundação de Apoio à Pesquisa do Estado de São Paulo (FAPESP) and 406710/2018-0 from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). NMS and CLR were supported by a fellowship from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) – Finance Code 001.