olecular basis of a bacterial-amphibian symbiosis revealed by comparative genomics, modeling, and functional testin

Author(s)

Brunetti, Andres E. ^{[1, 2]} ; Bunk, Boyke ^[3] ; Lyra, Mariana L. ^{[4, 5]} ; Fuzo, Carlos A. ^[6] ; Marani, Mariela M. ^[7] ; Sproeer, Cathrin ^[3] ; Haddad, Celio F. B. ^{[4, 5]} ; Lopes, Norberto P. ^[1] ; Overmann, Joerg ^{[3, 8]}

Affiliation

^[1] Univ Sao Paulo, Fac Ciencias Farmaceut Ribeirao Preto, Dept Ciencias BioMol, BR-14040903 Ribeirao Preto, SP - Brazil

^[2] Univ Nacl Misiones, Fac Ciencias Exactas, Inst Biol Subtrop CONICET UNaM, Lab Genet Evolut, RA-3300 Posadas - Argentina

^[3] Leibniz Inst DSMZ German Collect Microorganisms &, D-38124 Braunschweig - Germany

^[4] Univ Estadual Paulista, Ctr Aquicultura, Inst Biociencias, BR-13506900 Rio Claro, SP - Brazil

^[5] Univ Estadual Paulista, Dept Biodiversidade, Inst Biociencias, BR-13506900 Rio Claro, SP - Brazil

^[6] Univ Sao Paulo, Fac Ciencias Farmaceut Ribeirao Preto, Dept Anal Clin Toxicol & Bromatol, BR-14040903 Ribeirao Preto, SP - Brazil

^[7] Consejo Nacl Invest Cient & Tecn, Inst Patagon Estudio Ecosistemas Continentales, IPEEC CONICET, U9120ACD, Puerto Madryn - Argentina

^[8] Tech Univ Carolo Wilhelmina Braunschweig, Mikrobiol, D-38106 Braunschweig - Germany

• Document type: Journal article
• Source: ISME Journal; v. 16, n. 3 OCT 2021.
• Web of Science Citations: 1

Abstract

The molecular bases for the symbiosis of the amphibian skin microbiome with its host are poorly understood. Here, we used the odor-producer Pseudomonas sp. MPFS and the treefrog Boana prasina as a model to explore bacterial genome determinants and the resulting mechanisms facilitating symbiosis. Pseudomonas sp. MPFS and its closest relatives, within a new clade of the P. fluoresens Group, have large genomes and were isolated from fishes and plants, suggesting environmental plasticity. We annotated 16 biosynthetic gene clusters from the complete genome sequence of this strain, including those encoding the synthesis of compounds with known antifungal activity and of odorous methoxypyrazines that likely mediate sexual interactions in Boana prasina. Comparative genomics of Pseudomonas also revealed that Pseudomonas sp. MPFS and its closest relatives have acquired specific resistance mechanisms against host antimicrobial peptides (AMPs), specifically two extra copies of a multidrug efflux pump and the same two-component regulatory systems known to trigger adaptive resistance to AMPs in P. aeruginosa. Subsequent molecular modeling indicated that these regulatory systems interact with an AMP identified in Boana prasina through the highly acidic surfaces of the proteins comprising their sensory domains. In agreement with a symbiotic relationship and a highly selective antibacterial function, this AMP did not inhibit the growth of Pseudomonas sp. MPFS but inhibited the growth of another Pseudomonas species and Escherichia coli in laboratory tests. This study provides deeper insights into the molecular interaction of the bacteria-amphibian symbiosis and highlights the role of specific adaptive resistance toward AMPs of the hosts. (AU)

• FAPESP's process: 20/02207-5 - Inventorying secondary metabolism applying metabolomic strategies: contribution to the Brazilian biodiversity valuation
• Grantee: Norberto Peporine Lopes
• Support Opportunities: BIOTA-FAPESP Program - Thematic Grants
• FAPESP's process: 13/50954-0 - Novel therapeutic agents from the bacterial symbionts of Brazilian invertebrates
• Grantee: Mônica Tallarico Pupo
• Support Opportunities: BIOTA-FAPESP Program - Thematic Grants
• FAPESP's process: 17/26162-8 - Diversity and conservation of Brazilian amphibians
• Grantee: Mariana Lúcio Lyra
• Support Opportunities: Scholarships in Brazil - Technical Training Program - Technical Training
• FAPESP's process: 17/23725-1 - Genomic Analysis of Skin Symbiotic Bacteria in Frogs as Potential Source of Volatile Compounds
• Grantee: Andrés Eduardo Brunetti
• Support Opportunities: Scholarships abroad - Research Internship - Post-doctor
• FAPESP's process: 14/20915-6 - Chemical ecology in anurans: characterization of volatile compounds and peptide pheromones from the skin secretions of frogs
• Grantee: Andrés Eduardo Brunetti
• Support Opportunities: Scholarships in Brazil - Post-Doctoral