Microbial Ecology

, Volume 76, Issue 3, pp 825–838 | Cite as

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

  • Cintia P. J. Rua
  • Louisi S. de Oliveira
  • Adriana Froes
  • Diogo A. Tschoeke
  • Ana Carolina Soares
  • Luciana Leomil
  • Gustavo B. Gregoracci
  • Ricardo Coutinho
  • Eduardo Hajdu
  • Cristiane C. Thompson
  • Roberto G. S. Berlinck
  • Fabiano L. Thompson
Invertebrate Microbiology


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.


Halogenases Sponges Metagenomics Holobiont Bromopyrrole alkaloids Horizontal gene transfer 



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 Information

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.].

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

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

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High Resolution Image (TIFF 5823 kb)
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Distribution of sequences with assigned functions in categories of subsystems—level 1 (GIF 263 kb)

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High Resolution Image (TIFF 2339 kb)
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ESM 3 (DOCX 22 kb)
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ESM 4 (DOCX 19 kb)
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ESM 5 (DOCX 588 kb)


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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Cintia P. J. Rua
    • 1
    • 2
  • Louisi S. de Oliveira
    • 2
  • Adriana Froes
    • 2
  • Diogo A. Tschoeke
    • 2
    • 3
  • Ana Carolina Soares
    • 2
  • Luciana Leomil
    • 2
  • Gustavo B. Gregoracci
    • 4
  • Ricardo Coutinho
    • 5
  • Eduardo Hajdu
    • 6
  • Cristiane C. Thompson
    • 2
  • Roberto G. S. Berlinck
    • 1
  • Fabiano L. Thompson
    • 1
  1. 1.Instituto de Química de São CarlosUniversidade de São PauloSão CarlosBrazil
  2. 2.Instituto de BiologiaUniversidade Federal do Rio de Janeiro (UFRJ)Rio de JaneiroBrazil
  3. 3.Núcleo em Ecologia e Desenvolvimento Sócio-Ambiental de Macaé (NUPEM)Universidade Federal do Rio de JaneiroMacaéBrazil
  4. 4.Departamento de Ciências do MarUniversidade Federal de São PauloSantosBrazil
  5. 5.Instituto de Estudos do Mar Almirante Paulo MoreiraArraial do CaboBrazil
  6. 6.Museu Nacional – UFRJDepartamento de Invertebrados. Laboratório de PoriferaRio de JaneiroBrazil

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