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

  • Invertebrate Microbiology
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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.

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Acknowledgements

We thank Karen J. Nicacio (PhD student at IQSC, USP) for help in the literature survey as well as the funding agencies CNPq, FAPERJ, CAPES, and FAPESP for financial support.

Funding

This work was supported by FAPERJ [CNE E-26/110.735/2013 to E.H.], CAPES [CIMAR 1986/2014 to E.H.] and FAPESP [BIOTA/BIOprospecTA grant 2013/50228-8 to R.G.S.B. and Post-Doctoral Scholarship 2014/17616- 7 to C.P.J.R.].

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Authors and Affiliations

  1. Instituto de Química de São Carlos, Universidade de São Paulo, Avenida Trabalhador São-carlense, 400, Caixa Postal 780 - CEP13560-970, São Carlos, SP, CEP 13566-590, Brazil

    Cintia P. J. Rua, Roberto G. S. Berlinck & Fabiano L. Thompson

  2. Instituto de Biologia, Universidade Federal do Rio de Janeiro (UFRJ), Av. Carlos Chagas Filho, s/ n° - CCS, Lab de Microbiologia – Bloco A (Anexo) A3 – sl 102, Rio de Janeiro, RJ, CEP 21941-599, Brazil

    Cintia P. J. Rua, Louisi S. de Oliveira, Adriana Froes, Diogo A. Tschoeke, Ana Carolina Soares, Luciana Leomil & Cristiane C. Thompson

  3. Núcleo em Ecologia e Desenvolvimento Sócio-Ambiental de Macaé (NUPEM), Universidade Federal do Rio de Janeiro, Av. São José Barreto, 764 - São José do Barreto, Macaé - RJ, Macaé, RJ, CEP 27965-045, Brazil

    Diogo A. Tschoeke

  4. Departamento de Ciências do Mar, Universidade Federal de São Paulo, Av. Alm. Saldanha da Gama, 89, Santos, CEP 11030-400, Brazil

    Gustavo B. Gregoracci

  5. Instituto de Estudos do Mar Almirante Paulo Moreira, Rua Kioto, 253, Praia dos Anjos, Arraial do Cabo, RJ, CEP 28930-000, Brazil

    Ricardo Coutinho

  6. Museu Nacional – UFRJ, Departamento de Invertebrados. Laboratório de Porifera, Quinta da Boa Vista, s/n. São Cristóvão, Rio de Janeiro, CEP 20940-040, Brazil

    Eduardo Hajdu

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  1. Cintia P. J. Rua
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Correspondence to Roberto G. S. Berlinck or Fabiano L. Thompson.

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Electronic Supplementary Material

ESM 1

Most abundant phyla/classes of Bacteria and Archaea found in metagenomes (GIF 186 kb)

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ESM 2

Distribution of sequences with assigned functions in categories of subsystems—level 1 (GIF 263 kb)

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Rua, C.P.J., de Oliveira, L.S., Froes, A. et al. Microbial and Functional Biodiversity Patterns in Sponges that Accumulate Bromopyrrole Alkaloids Suggest Horizontal Gene Transfer of Halogenase Genes. Microb Ecol 76, 825–838 (2018). https://doi.org/10.1007/s00248-018-1172-6

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  • DOI: https://doi.org/10.1007/s00248-018-1172-6

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