Fluxes of the Amazon River plume nutrients and microbes into marine sponges

Tatiane A de Menezes; Mayanne A M de Freitas; Michele S Lima; Ana Carolina Soares; Camille Leal; Mileane de S Busch; Diogo A Tschoeke; Luciana de O Vidal; Georgia C Atella; Ricardo H Kruger; João Setubal; Agnaldo A Vasconcelos; Michel M de Mahiques; Eduardo Siegle; Nils Edvin Asp; Carlos Cosenza; Eduardo Hajdu; Carlos E de Rezende; Cristiane C Thompson; Fabiano L Thompson

doi:10.1016/j.scitotenv.2022.157474

Fluxes of the Amazon River plume nutrients and microbes into marine sponges

Sci Total Environ. 2022 Nov 15:847:157474. doi: 10.1016/j.scitotenv.2022.157474. Epub 2022 Jul 20.

Authors

Tatiane A de Menezes¹, Mayanne A M de Freitas¹, Michele S Lima¹, Ana Carolina Soares², Camille Leal¹, Mileane de S Busch³, Diogo A Tschoeke⁴, Luciana de O Vidal⁵, Georgia C Atella³, Ricardo H Kruger⁶, João Setubal², Agnaldo A Vasconcelos⁷, Michel M de Mahiques⁸, Eduardo Siegle⁸, Nils Edvin Asp⁹, Carlos Cosenza¹⁰, Eduardo Hajdu¹¹, Carlos E de Rezende¹², Cristiane C Thompson¹³, Fabiano L Thompson¹⁴

Affiliations

¹ Laboratory of Microbiology, Biology Institute, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro, Brazil.
² Bioinformatics Laboratory, Department of Biochemistry, Institute of Chemistry, University of São Paulo (USP), São Paulo, Brazil.
³ Laboratory of Lipids Biochemistry and Lipoprotein, Biochemistry Institute Leopoldo de Meis, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro, Brazil.
⁴ Biomedical Engineering Program - COPPE, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro, Brazil.
⁵ Environmental Sciences Laboratory, Biosciences and Biotechnology Center, Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF), Campos dos Goytacazes, Rio de Janeiro, Brazil; Department of Ecology and Marine Resources, Institute of Biosciences, Universidade Federal do Estado do Rio de Janeiro (UNIRIO), Rio de Janeiro, Brazil.
⁶ Laboratory of Enzymology, University of Brasilia (UNB), Brasilia, Brazil.
⁷ Greenpeace Brazil, Rio de Janeiro, Brazil.
⁸ Oceanographic Institute (IO), University of São Paulo (USP), São Paulo, Brazil.
⁹ Federal University of Pará, Institute of Coastal Studies (IECOS), Bragança Campus, Bragança, PA, Brazil.
¹⁰ Center of Technology - CT2, SAGE-COPPE, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro, Brazil.
¹¹ Department of Invertebrates, National Museum, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro, Brazil.
¹² Environmental Sciences Laboratory, Biosciences and Biotechnology Center, Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF), Campos dos Goytacazes, Rio de Janeiro, Brazil. Electronic address: crezende@uenf.br.
¹³ Laboratory of Microbiology, Biology Institute, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro, Brazil. Electronic address: thompsoncristiane@gmail.com.
¹⁴ Laboratory of Microbiology, Biology Institute, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro, Brazil; Center of Technology - CT2, SAGE-COPPE, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro, Brazil. Electronic address: fabianothompson1@gmail.com.

PMID: 35868367
DOI: 10.1016/j.scitotenv.2022.157474

Abstract

Sponges have co-evolved with microbes for over 400 myr. Previous studies have demonstrated that sponges can be classified according to the abundance of microbes in their tissues as Low Microbial Abundance (LMA) and High Microbial Abundance (HMA). While LMA sponges rely mainly on water column microbes, HMA appear to rely much more on symbiotic fermentative and autotrophic microbes maintained in their tissues. However, it is unclear if this pattern holds when comparing different species of tropical sponges under extreme nutrient conditions and sediment loads in the water column, such as the Great Amazon Reef System (GARS), which covers an area of ~56,000 km² off the Amazon River mouth. Sponges are the major GARS benthic components. However, these sponges' microbiome across the GARS is still unknown. Here, we investigated water quality, isotopic values (δ¹³C and δ¹⁵N), metagenomic and lipidomic profiles of sponges obtained from different sectors throughout the GARS. >180 million shotgun metagenomic reads were annotated, covering 22 sponge species. Isotopic and lipidomic analyses suggested LMA sponges rely on the Amazon River Plume for nutrition. HMA sponges (N = 15) had higher Roseiflexus and Nitrospira abundance, whereas LMA sponges (N = 7) had higher Prochlorococcus and Pelagibacter abundance. Functional data revealed that the LMA sponge microbiomes had greater number of sequences related to phages and prophages as well as electron transport and photophosphorylation which may be related to photosynthetic processes associated with the Prochlorococcus and Synechococcus found in the LMA. The higher phages abundance in LMA sponges could be related to these holobionts' reduced defense towards phage infection. Meanwhile, HMA sponge microbiomes had higher Clustered Regularly Interspaced Short Palindromic Repeats-CRISPR abundance, which may be involved in defense against phage infection. This study sheds light on the nutrient fluxes and microbes from the Amazon River plume into the sponge holobionts.

Keywords: Biomarkers; Isotopic features; Lipidomics; Marine sponges; Metagenomics.

MeSH terms

Animals
Nutrients
Phylogeny
Porifera*
RNA, Ribosomal, 16S
Rivers*

Substances

RNA, Ribosomal, 16S