Microbial and Functional Biodiversity Patterns in Sponges that Accumulate Bromopyrrole Alkaloids Suggest Horizontal Gene Transfer of Halogenase Genes

Author(s):Show less -

Rua, Cintia P. J. ^{[1, 2]} ; de Oliveira, Louisi S. ^[1] ; Froes, Adriana ^[1] ; Tschoeke, Diogo A. ^{[1, 3]} ; Soares, Ana Carolina ^[1] ; Leomil, Luciana ^[1] ; Gregoracci, Gustavo B. ^[4] ; Coutinho, Ricardo ^[5] ; Hajdu, Eduardo ^[6] ; Thompson, Cristiane C. ^[1] ; Berlinck, Roberto G. S. ^[2] ; Thompson, Fabiano L. ^[2]

Affiliation

^[1] Univ Fed Rio de Janeiro, Inst Biol, CCS, Lab Microbiol, Av Carlos Chagas Filho S-N, BR-21941599 Rio De Janeiro, RJ - Brazil

^[2] Univ Sao Paulo, Inst Quim Sao Carlos, Ave Trabalhador Sao Carlense 400, Caixa Postal 780, BR-13566970 Sao Carlos, SP - Brazil

^[3] Univ Fed Rio de Janeiro, Nucleo Ecol & Desenvolvimento Socioambiental Maca, Av Sao Jose Barreto, 764 Sao Jose do Barreto, BR-27965045 Macae, RJ - Brazil

^[4] Univ Fed Sao Paulo, Dept Ciencias Mar, Av Alm Saldanha da Gama 89, BR-11030400 Santos - Brazil

^[5] Inst Estudos Mar Almirante Paulo Moreira, Rua Kioto 253, BR-28930000 Arraial Do Cabo, RJ - Brazil

^[6] Museu Nacl UFRJ, Dept Invertebrados, Lab Porifera, S-N Sao Cristovao, BR-20940040 Rio De Janeiro - Brazil

• Document type: Journal article
• Source: MICROBIAL ECOLOGY; v. 76, n. 3, p. 825-838, OCT 2018.
• Web of Science Citations: 3

Abstract

Marine sponge holobionts harbor complex microbial communities whose members may be the true producers of secondary metabolites accumulated by sponges. Bromopyrrole alkaloids constitute a typical class of secondary metabolites isolated from sponges that very often display biological activities. Bromine incorporation into secondary metabolites can be catalyzed by either halogenases or haloperoxidases. The diversity of the metagenomes of sponge holobiont species containing bromopyrrole alkaloids (Agelas spp. and Tedania brasiliensis) as well as holobionts devoid of bromopyrrole alkaloids spanning in a vast biogeographic region (approx. Seven thousand km) was studied. The origin and specificity of the detected halogenases was also investigated. The holobionts Agelas spp. and T brasiliensis did not share microbial halogenases, suggesting a species-specific pattern. Bacteria of diverse phylogenetic origins encoding halogenase genes were found to be more abundant in bromopyrrole-containing sponges. The sponge holobionts (e.g., Agelas spp.) with the greatest number of sequences related to clustered, interspaced, short, palindromic repeats (CRISPRs) exhibited the fewest phage halogenases, suggesting a possible mechanism of protection from phage infection by the sponge host. This study highlights the potential of phages to transport halogenases horizontally across host sponges, particularly in more permissive holobiont hosts, such as Tedania spp. (AU)

• FAPESP's process: 14/17616-7 - Phylogenetic and functional characterization of microbial communities associated with sponges that present bromopyrrole alkaloids and characterization of gene clusters which include nonribossomal peptide synthetase (NRPS)
• Grantee: Cintia Paula Jandre Rua
• Support Opportunities: Scholarships in Brazil - Post-Doctoral
• FAPESP's process: 13/50228-8 - Biodiversity components, and their metabolic characters, of Brazilian Islands: an integrated approach
• Grantee: Roberto Gomes de Souza Berlinck
• Support Opportunities: BIOTA-FAPESP Program - Thematic Grants