THE AMPHIBIAN SKIN MICROBIOME

The skin microbiome of amphibians has been shown to play an important role in the protection of their hosts from pathogenic organisms. Some members of this microbiome are able to inhibit, in vivo and in vitro, the growth of the pathogenic fungi Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal). These fungi cause the emerging disease known as chytridiomycosis that has led to dramatic population declines and extinctions of amphibians worldwide.

Recent studies have shown that skin bacterial communities in amphibians are influenced by different biotic and abiotic factors. In my laboratory, we are interested in determining:
1) What biotic and abiotic factors influence the structure and function of skin microbial communities?
2) By what mechanisms does the host modulate the structure and function of its microbiome?
3) How do interactions within the microbial community determine emergent properties such as protection from pathogens?

Through the use of massive sequencing technologies and classical culture methods, we are addressing these and other questions with the goal of understanding the ecological and evolutionary bases that give rise to the symbiosis between amphibians and microorganisms. Our study models are mainly Mexican amphibian species, including endemic species at risk of extinction, such as the ajolotes of the genus Ambystoma.

Related publications

  • Rebollar EA, Martínez-Ugalde E, Orta AH. (2020). The amphibian skin microbiome and its protective role against chytridiomycosis. Herpetologica, 76 (2), 167-177. https://doi.org/10.1655/0018-0831-76.2.167.
  • Ramírez-Barahona S, González-Serrano FM, Martínez-Ugalde E, Soto-Pozos A, Parra-Olea G,  Rebollar EA. (2023). Host phylogeny and environment shape the diversity of salamander skin bacterial communities. Anim Microbiome. 5, 52. https://doi.org/10.1186/s42523-023-00271-7

THE MICROBIOME OF AMBYSTOMA ALTAMIRANI: A STUDY OF BIOTIC AND ABIOTIC FACTORS INFLUENCING THE SYMBIONT MICROBIOTA OF THE SKIN OF THE MOUNTAIN BROOK SALAMANDER

In this project we aim to describe for the first time the skin microbiota of Ambystoma altamirani. This paedomorph aquatic salamander lives in the Sierra de Cruces, a mountain range that provides environmental services to central Mexico. A. altamirani is highly threatened due to habitat loss, pollution, and the introduction of exotic species. We want to determine the factors that determine the structure and function of the skin microbiota in this species. Abiotic factors include water physicochemical variables over four seasons.

Related publications

  • Basanta D, Betancourt-León O, Chávez OL, Pérez-Torres A, Rebollar EA, Martínez-Ugalde E, Ávila-Akerberg VD, González Martínez TM, Vázquez Trejo M, Parra-Olea G. (2021) Batrachochytrium dendrobatidis occurrence in dead amphibians of central mexico: a report of Ambystoma altamirani and Lithobates montezumae. Revista Latinoamericana de Herpetología, Vol.04 No.01 / Mayo 2021. 
  • Basanta MD, Anaya-Morales SL, Martínez-Ugalde E, González Martínez TM, Ávila-Akerberg VD, Trejo MV and Rebollar EA. (2022) Metamorphosis and seasonality are major determinants of chytrid infection in a paedomorphic salamander. Animal Conservation. https://doi.org/10.1111/acv.12824.
  • Martínez-Ugalde E, Ávila-Akerberg V, González Martínez TM, Vázquez Trejo M, Zavala Hernández D, Anaya-Morales SL, Rebollar EA (2022) The skin microbiota of the axolotl Ambystoma altamirani is highly influenced by metamorphosis and seasonality but not by pathogen infection. Anim Microbiome. 4(1):63. doi: 10.1186/s42523-022-00215-7. 
  • Martínez-Ugalde E, Ávila-Akerberg V, González Martínez TM, Rebollar EA. Gene functions of the Ambystoma altamirani skin microbiome vary across space and time but potential antifungal genes are widespread and prevalent. Microb Genom. 2024 Jan;10(1):001181. doi: 10.1099/mgen.0.001181.

DECIPHERING THE AXOLOTL SKIN MICROBIOME AND THE CONSEQUENCES OF HOST-MICROBIOME INTERACTIONS FOR A LETHAL EMERGING DISEASE

This project aims to determine whether host-associated genetic factors (genetic diversity, demographic history, and immune response) modulate the diversity and structure of skin microbial communities in species of salamanders (Ambystoma) endemic to the Transmexican Volcanic Belt. With this information, we will also determine whether the incidence of the pathogenic fungi Batrachochytrium dendrobatidis (Bd) and B. salamandrivorans (Bsal) are associated with specific combinations of host-associated factors or their skin microbiomes.

In this work we analyzed cutaneous microbial diversity, host genomic diversity, diversity of antimicrobial peptide secretions (AMPs), and the incidence of Bd and Bsal pathogens. Our study systems are eight species of salamanders endemic to the Neovolcanic Transversal Axis of Mexico: Ambystoma altamirani, A. ordinarium, A. dumerilii, A. andersoni, A. granulosum, A. velasci, A. mexicanum and A. taylori. These species have restricted distribution in lagoons and rivers, and are in some category of risk by Mexican Law NOM-059-Semarnat-2010 and the IUCN.

We are evaluating for the first time the skin microbiome (bacteria and fungi) and the secretion of antimicrobial peptides in wild salamander populations. We also evaluate polymorphisms (SNPs) in the genome of the eight species of salamanders. SNP detection will be an essential tool to link patterns between the genetic diversity and demographic history of salamanders with the diversity of the skin microbiome and the incidence of pathogenic fungi. The integration of these data will allow us to propose conservation strategies for these threatened or endangered salamander species.

Related publications

  • Basanta MD, Avila-Akerberg V, Byrne AQ, Castellanos-Morales G, González Martínez TM, Maldonado-López Y, Rosenblum EB, Suazo-Ortuño I, Parra Olea G, Rebollar EA. (2022) The fungal pathogen Batrachochytrium salamandrivorans is not detected in wild and captive amphibians from Mexico. PeerJ. Oct 3;10:e14117. doi: 10.7717/peerj.14117.
  • Soto-Cortés, E., Marroquín-Rodríguez, M., Basanta, M.D. Yurixhi Maldonado-López, Gabriela Parra-Olea, Eria A. Rebollar. Host Species and Environment Shape the Skin Microbiota of Mexican Axolotls. Microb Ecol 87, 98 (2024). https://doi.org/10.1007/s00248-024-02411-1.

THE SKIN OF MEXICAN AXOLOTLS AS A SOURCE OF BACTERIA AND COMPOUNDS WITH ANTIMICROBIAL ACTIVITY

The amphibian mucosa constitutes the first layer of defense against pathogenic microorganisms. The composition of the mucosa is a combination of host-secreted molecules (including antimicrobial peptides – AMPs) and a complex community of skin-associated microorganisms.
In our laboratory, and in collaboration with other research groups, we have identified bacteria from the skin microbiota of the axolotl Ambystoma altamirani that have antibacterial or antifungal activity. Antibacterial activity has been observed against priority human pathogens (such as Staphylococcus aureus, Pseudomonas aeruginosa and Acinetobacter baumannii), including antibiotic-resistant strains, while antifungal activity has been demonstrated against the fungus Bd but also against the phytopathogenic fungus Botryitis cinerea (causing grey mould in tomato, strawberry and other crops).
In addition to the protection provided by the skin microbiota, many AMPs with antifungal capacities have been isolated from the skin secretions of frogs, but very few have been isolated from salamanders and none from axolotls. In the laboratory, we have obtained peptide secretions from the skin of eight species of axolotls with the aim of beginning to characterize their antimicrobial properties.
In summary, we consider that axolotl skin represents a source with great potential for the identification of new antimicrobials against clinical pathogens, as well as against pathogens that threaten wildlife and plants of agricultural interest.
In this project we seek, from the skin of axolotls:
(1) identify bacteria or compounds that have activity against human pathogenic bacteria or against pathogenic fungi of amphibians or plants of agricultural interest
(2) analyze the identity of bacteria with antimicrobial activity using genomics and describe the molecular bases of this phenotype, and finally
(3) delve deeper into the chemical identity of compounds with antimicrobial activity found to be secreted by bacteria or secreted by axolotls.

Related Publications

  • Cevallos MA, Basanta MD, Bello-López E, Escobedo-Muñoz AS, González-Serrano FM,  Nemec A, Romero-Contreras A, Serrano M, Rebollar EA (2022) Genomic characterization of antifungal Acinetobacter bacteria isolated from the skin of the frogs Agalychnis callidryas and Craugastor fitzingeri, FEMS Microbiology Ecology, Volume 98, Issue 12, December 2022, fiac126, https://doi.org/10.1093/femsec/fiac126.
  • Romero-Contreras YJ, Gonzalez-Serrano F, Formey D, Aragón W, Chacón FI, Torres M, Cevallos MÁ, Dib JR, Rebollar EA, Serrano M. Amphibian skin bacteria display antifungal activity and induce plant defense mechanisms against Botrytis cinerea. Front Plant Sci. 2024 Apr 9;15:1392637. doi: 10.3389/fpls.2024.1392637. 
  • Romero-Contreras, Y.J., González-Serrano, F., Bello-López, E. Damien Formey, Wendy Aragón, Miguel Ángel Cevallos, Eria A. Rebollar, Mario Serrano. Bacteria from the skin of amphibians promote growth of Arabidopsis thaliana and Solanum lycopersicum by modifying hormone-related transcriptome response. Plant Mol Biol114, 39 (2024). https://doi.org/10.1007/s11103-024-01444-x

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