Characterization of the bacterial microbiome of non-hematophagous bats and associated ectoparasites from Brazil

Marcos Rogério André; Priscila Ikeda; Daniel Antônio Braga Lee; Renan Bressianini do Amaral; Lucas Amoroso Lopes Carvalho; Daniel Guariz Pinheiro; Jaire Marinho Torres; Victória Valente Califre de Mello; Gregory K Rice; Regina Z Cer; Elizabete Captivo Lourenço; Carisa Elisei Oliveira; Heitor Miraglia Herrera; Darci Moraes Barros-Battesti; Rosangela Zacarias Machado; Kimberly A Bishop-Lilly; Clifton L Dalgard; J Stephen Dumler

doi:10.3389/fmicb.2023.1261156

Characterization of the bacterial microbiome of non-hematophagous bats and associated ectoparasites from Brazil

Front Microbiol. 2023 Oct 19:14:1261156. doi: 10.3389/fmicb.2023.1261156. eCollection 2023.

Authors

Marcos Rogério André¹, Priscila Ikeda¹, Daniel Antônio Braga Lee¹, Renan Bressianini do Amaral¹, Lucas Amoroso Lopes Carvalho², Daniel Guariz Pinheiro², Jaire Marinho Torres³, Victória Valente Califre de Mello¹, Gregory K Rice^{4

5}, Regina Z Cer⁵, Elizabete Captivo Lourenço⁶, Carisa Elisei Oliveira³, Heitor Miraglia Herrera³, Darci Moraes Barros-Battesti¹, Rosangela Zacarias Machado¹, Kimberly A Bishop-Lilly⁵, Clifton L Dalgard⁷, J Stephen Dumler⁸

Affiliations

¹ Vector-Borne Bioagents Laboratory (VBBL), Departamento de Patologia, Reprodução e Saúde Única, Faculdade de Ciências Agrárias e Veterinárias (FCAV), Universidade Estadual Paulista (UNESP), Jaboticabal, São Paulo, Brazil.
² Departamento de Biotecnologia Ambiental e Agropecuária, Faculdade de Ciências Agrárias e Veterinárias (FCAV), Universidade Estadual Paulista (UNESP), Jaboticabal, São Paulo, Brazil.
³ Laboratório de Biologia Parasitária, Programa de Pós-Graduação em Biotecnologia, Universidade Católica Dom Bosco, Campo Grande, Mato Grosso do Sul, Brazil.
⁴ Leidos, Inc., Reston, VA, United States.
⁵ Department of Genomics and Bioinformatics, Naval Medical Research Command, Fort Detrick, Frederick, MD, United States.
⁶ Laboratório de Ecologia de Mamíferos, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil.
⁷ The American Genome Center, Center for Military Precision Health and Department of Anatomy, Physiology, and Genetics, Uniformed Services University of the Health Sciences, Bethesda, MD, United States.
⁸ Department of Pathology, University of the Health Sciences, Bethesda, MD, United States.

Abstract

Introduction: Bats, along with their ectoparasites, harbor a wide diversity of symbiotic and potential pathogenic bacteria. Despite the enormous diversity of bats (181 species), few studies aimed to investigate the bacterial microbiome of Brazilian chiropterans and associated ectoparasites. This study aimed to characterize the bacterial microbiome of non-hematophagous bats and associated Streblidae flies and Macronyssidae and Spinturnicidae mites in the state of Mato Grosso do Sul, midwestern Brazil.

Methods: Oral and rectal swabs were collected from 30 bats (Artibeus lituratus [n = 13], Artibeus planirostris [n = 9], Eptesicus furinalis [n = 5], Carollia perspicillata [n = 2], and Platyrrhinus lineatus [n = 1]). In addition, a total of 58 mites (15 Macronyssidae and 43 Spinturnicidae) and 48 Streblidae bat flies were collected from the captured bats. After DNA extraction and purification, each sample's bacterial composition was analyzed with metagenomic sequencing.

Results: The microbiome composition of both oral and rectal bat swab samples showed that Gammaproteobacteria was the most abundant bacterial class. Spiroplasma, Wolbachia and Bartonella represented the most abundant genera in Streblidae flies. While Wolbachia (Alphaproteobacteria) was the most abundant genus found in Spinturnicidae, Arsenophonus (Gammaproteobacteria) was found in high abundance in Macronyssidae mites. In addition to characterizing the microbiome of each sample at the class and genus taxonomic levels, we identified medically significant bacteria able to infect both animals and humans in oral (Streptococcus and Anaplasma) and rectal swabs (Enterobacter, Klebsiella, Escherichia, Enterococcus, Streptococcus), Macronyssidae (Anaplasma, Bartonella, Ehrlichia) and Spinturnicidae (Anaplasma, Bartonella) mites as well as Streblidae flies (Spiroplasma, Bartonella).

Discussion and conclusion: Besides expanding the knowledge on the bacterial microbiome of non-hematophagous bats and Streblidae flies from Brazil, the present work showed, for the first time, the bacterial community of bat-associated Macronyssidae and Spinturnicidae mites.

Keywords: Chiroptera; Macronyssidae; Spinturnicidae; Streblidae; bat flies; microbiome composition; mites.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was funded by FAPESP (Fundação de Amparo à Pesquisa do Estado da São Paulo – Process 2022/05615-2) and CNPq (National Council for Scientific and Technological Development; Productivity Grant to MA [CNPq Process #303701/2021-8]). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001. PI (2017/13557-4; 2019/13232-3), DL (2022/07008-6), and RA (2018/19672-2) were graduate students supported by FAPESP. Funding was provided to support technical components of the research in part from the U.S. Department of Defense for the Uniformed Services University PAT-74-3977 to JD and HU0001222014 to CD. The work at NMRC was supported by the Armed Forces Health Surveillance Division (AFHSD), Global Emerging Infections Surveillance (GEIS) Branch, ProMIS ID P0167_22_NM to KB-L and Navy WUN A1417.