Species-specific relationships between deep sea sponges and their symbiotic Nitrosopumilaceae

Alessandro N. Garritano; Marwan E. Majzoub; Barbara Ribeiro; Taissa Damasceno; Fluvio Modolon; Camila Messias; Caren Vilela; Gustavo A. S. Duarte; Lilian Hill; Raquel S Peixoto; Torsten Thomas

doi:10.1038/s41396-023-01439-4

Species-specific relationships between deep sea sponges and their symbiotic Nitrosopumilaceae

Alessandro N. Garritano, Marwan E. Majzoub, Barbara Ribeiro, Taissa Damasceno, Fluvio Modolon, Camila Messias, Caren Vilela, Gustavo A. S. Duarte, Lilian Hill, Raquel S Peixoto, Torsten Thomas

Research output: Contribution to journal › Article › peer-review

5 Scopus citations

Abstract

Sponges thrive in the deep, dark and nutrient-depleted ocean and may rely on microbial symbionts for carbon acquisition and energy generation. However, these symbiotic relationships remain largely unexplored. In this study, we analyze the microbiome of deep-sea sponges and show that ammonia-oxidizing archaea (AOA) of the family Nitrosopumilaceae make up at least 75% of the microbial communities of the sponges Aphrocallistes sp., Farrea sp. and Paratimea sp.. Given the known autotrophic metabolism of AOAs, this implies that these sponge holobionts can have the capacity for primary production in the deep-sea. We also show that specific AOA lineages are highly specific towards their hosts, hinting towards an unprecedent vertical transmission of these symbionts in deep-sea sponges. Our results show that the ecology and evolution of symbiotic relationships in deep-sea sponge is distinct from that of their shallow-water counterparts.

Original language	English (US)
Journal	The ISME Journal
DOIs	https://doi.org/10.1038/s41396-023-01439-4
State	Published - May 31 2023

Bibliographical note

KAUST Repository Item: Exported on 2023-06-06
Acknowledged KAUST grant number(s): BAS/1/1095-01-01
Acknowledgements: Open Access funding enabled and organized by CAUL and its Member Institutions. This paper was carried out in association with the ongoing R&D project registered as ANP 21005-4, “PROBIO-DEEP – Survey of potential impacts caused by oil and gas exploration on deep-sea marine holobionts and selection of potential bioindicators and bioremediation processes for these ecosystems” (UFRJ/Shell Brasil/ANP), sponsored by Shell Brasil under the ANP R&D levy as “Compromisso de Investimentos com Pesquisa e Desenvolvimento”. R.S.P. was also supported through KAUST grant number BAS/1/1095-01-01.

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics

Access to Document

10.1038/s41396-023-01439-4

https://repository.kaust.edu.sa/bitstream/10754/692379/1/s41396-023-01439-4.pdf

Cite this

@article{e062ad2e48944276961bfb67aa68894a,

title = "Species-specific relationships between deep sea sponges and their symbiotic Nitrosopumilaceae",

abstract = "Sponges thrive in the deep, dark and nutrient-depleted ocean and may rely on microbial symbionts for carbon acquisition and energy generation. However, these symbiotic relationships remain largely unexplored. In this study, we analyze the microbiome of deep-sea sponges and show that ammonia-oxidizing archaea (AOA) of the family Nitrosopumilaceae make up at least 75% of the microbial communities of the sponges Aphrocallistes sp., Farrea sp. and Paratimea sp.. Given the known autotrophic metabolism of AOAs, this implies that these sponge holobionts can have the capacity for primary production in the deep-sea. We also show that specific AOA lineages are highly specific towards their hosts, hinting towards an unprecedent vertical transmission of these symbionts in deep-sea sponges. Our results show that the ecology and evolution of symbiotic relationships in deep-sea sponge is distinct from that of their shallow-water counterparts.",

author = "Garritano, {Alessandro N.} and Majzoub, {Marwan E.} and Barbara Ribeiro and Taissa Damasceno and Fluvio Modolon and Camila Messias and Caren Vilela and Duarte, {Gustavo A. S.} and Lilian Hill and Peixoto, {Raquel S} and Torsten Thomas",

note = "KAUST Repository Item: Exported on 2023-06-06 Acknowledged KAUST grant number(s): BAS/1/1095-01-01 Acknowledgements: Open Access funding enabled and organized by CAUL and its Member Institutions. This paper was carried out in association with the ongoing R&D project registered as ANP 21005-4, “PROBIO-DEEP – Survey of potential impacts caused by oil and gas exploration on deep-sea marine holobionts and selection of potential bioindicators and bioremediation processes for these ecosystems” (UFRJ/Shell Brasil/ANP), sponsored by Shell Brasil under the ANP R&D levy as “Compromisso de Investimentos com Pesquisa e Desenvolvimento”. R.S.P. was also supported through KAUST grant number BAS/1/1095-01-01.",

year = "2023",

month = may,

day = "31",

doi = "10.1038/s41396-023-01439-4",

language = "English (US)",

journal = "The ISME Journal",

issn = "1751-7362",

publisher = "Nature Publishing Group",

}

TY - JOUR

T1 - Species-specific relationships between deep sea sponges and their symbiotic Nitrosopumilaceae

AU - Garritano, Alessandro N.

AU - Majzoub, Marwan E.

AU - Ribeiro, Barbara

AU - Damasceno, Taissa

AU - Modolon, Fluvio

AU - Messias, Camila

AU - Vilela, Caren

AU - Duarte, Gustavo A. S.

AU - Hill, Lilian

AU - Peixoto, Raquel S

AU - Thomas, Torsten

N1 - KAUST Repository Item: Exported on 2023-06-06 Acknowledged KAUST grant number(s): BAS/1/1095-01-01 Acknowledgements: Open Access funding enabled and organized by CAUL and its Member Institutions. This paper was carried out in association with the ongoing R&D project registered as ANP 21005-4, “PROBIO-DEEP – Survey of potential impacts caused by oil and gas exploration on deep-sea marine holobionts and selection of potential bioindicators and bioremediation processes for these ecosystems” (UFRJ/Shell Brasil/ANP), sponsored by Shell Brasil under the ANP R&D levy as “Compromisso de Investimentos com Pesquisa e Desenvolvimento”. R.S.P. was also supported through KAUST grant number BAS/1/1095-01-01.

PY - 2023/5/31

Y1 - 2023/5/31

N2 - Sponges thrive in the deep, dark and nutrient-depleted ocean and may rely on microbial symbionts for carbon acquisition and energy generation. However, these symbiotic relationships remain largely unexplored. In this study, we analyze the microbiome of deep-sea sponges and show that ammonia-oxidizing archaea (AOA) of the family Nitrosopumilaceae make up at least 75% of the microbial communities of the sponges Aphrocallistes sp., Farrea sp. and Paratimea sp.. Given the known autotrophic metabolism of AOAs, this implies that these sponge holobionts can have the capacity for primary production in the deep-sea. We also show that specific AOA lineages are highly specific towards their hosts, hinting towards an unprecedent vertical transmission of these symbionts in deep-sea sponges. Our results show that the ecology and evolution of symbiotic relationships in deep-sea sponge is distinct from that of their shallow-water counterparts.

AB - Sponges thrive in the deep, dark and nutrient-depleted ocean and may rely on microbial symbionts for carbon acquisition and energy generation. However, these symbiotic relationships remain largely unexplored. In this study, we analyze the microbiome of deep-sea sponges and show that ammonia-oxidizing archaea (AOA) of the family Nitrosopumilaceae make up at least 75% of the microbial communities of the sponges Aphrocallistes sp., Farrea sp. and Paratimea sp.. Given the known autotrophic metabolism of AOAs, this implies that these sponge holobionts can have the capacity for primary production in the deep-sea. We also show that specific AOA lineages are highly specific towards their hosts, hinting towards an unprecedent vertical transmission of these symbionts in deep-sea sponges. Our results show that the ecology and evolution of symbiotic relationships in deep-sea sponge is distinct from that of their shallow-water counterparts.

UR - http://hdl.handle.net/10754/692379

UR - https://www.nature.com/articles/s41396-023-01439-4

U2 - 10.1038/s41396-023-01439-4

DO - 10.1038/s41396-023-01439-4

M3 - Article

C2 - 37258653

SN - 1751-7362

JO - The ISME Journal

JF - The ISME Journal

ER -

Species-specific relationships between deep sea sponges and their symbiotic Nitrosopumilaceae

Abstract

Bibliographical note

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this