Responses of Coastal Marine Microbiomes Exposed to Anthropogenic Dissolved Organic Carbon

13 pages, 5 figures, supporting information https://doi.org/10.1021/acs.est.0c07262

Coastal seawaters receive thousands of organic pollutants. However, we have little understanding of the response of microbiomes to this pool of anthropogenic dissolved organic carbon (ADOC). In this study, coastal microbial communities were challenged with ADOC at environmentally relevant concentrations. Experiments were performed at two Mediterranean sites with different impact by pollutants and nutrients: off the Barcelona harbor (“BCN”), and at the Blanes Bay (“BL”). ADOC additions stimulated prokaryotic leucine incorporation rates at both sites, indicating the use of ADOC as growth substrate. The percentage of “membrane-compromised” cells increased with increasing ADOC, indicating concurrent toxic effects of ADOC. Metagenomic analysis of the BCN community challenged with ADOC showed a significant growth of Methylophaga and other gammaproteobacterial taxa belonging to the rare biosphere. Gene expression profiles showed a taxon-dependent response, with significantly enrichments of transcripts from SAR11 and Glaciecola spp. in BCN and BL, respectively. Further, the relative abundance of transposon-related genes (in BCN) and transcripts (in BL) correlated with the number of differentially abundant genes (in BCN) and transcripts (in BLA), suggesting that microbial responses to pollution may be related to pre-exposure to pollutants, with transposons playing a role in adaptation to ADOC. Our results point to a taxon-specific response to low concentrations of ADOC that impact the functionality, structure and plasticity of the communities in coastal seawaters. This work contributes to address the influence of pollutants on microbiomes and their perturbation to ecosystem services and ocean health.

This work was supported by the Spanish Ministry of Economy and Competitiveness (MEIC) through projects ISOMICS (CTM2015-65691-R) and REMARCA (CTM2012-34673). E.C.G. was supported by Agència de Gestió d’Ajuts Universtaris i Recerca, Generalitatde Catalunya (FI AGAUR) Scholarship, Generalitat de Catalunya Fellowship Program (Catalan Government, Generalitat de Catalunya) and by a “FORD ESPAÑA-APADRINA LA CIENCIA” contract. The research group of Global Change and Genomic Biogeochemistry is supported by the Catalan Government (2017SGR800). We thank Dr. J. M. Gasol for support with flow cytometry counts. Inorganic nutrient analyses were performed by M. I. Abad in coordination with Dr. E. Berdalet (Head of the Service) at the “Nutrient Analysis Service of the ICM-CSIC. Dr Piña is acknowledged for fruitful discussions.

With the funding support of the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S), of the Spanish Research Agency (AEI).

Peer reviewed