Extracellular DNA as a genetic recorder of microbial diversity in benthic deep-sea ecosystems

C Corinaldesi,A Dell’Anno,M Tangherlini,E Manea

doi:10.1038/s41598-018-20302-7

C Corinaldesi, A Dell’Anno + Show 2 more

Open Access

https://doi.org/10.1038/s41598-018-20302-7

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Abstract

Extracellular DNA in deep-sea sediments represents a major repository of genes, which previously belonged to living organisms. However, the extent to which these extracellular genes influence current estimates of prokaryotic biodiversity is unknown. We investigated the abundance and diversity of 16S rDNA sequences contained within extracellular DNA from continental margins of different biogeographic regions. We also compared the taxonomic composition of microbial assemblages through the analysis of extracellular DNA and DNA associated with living cells. 16S rDNA contained in the extracellular DNA pool contributed up to 50% of the total 16S rDNA copy number determined in the sediments. Ca. 4% of extracellular Operational Taxonomic Units (OTUs) were shared among the different biogeographic regions revealing the presence of a core of preserved OTUs. A higher fraction of OTUs was exclusive of each region potentially due to its geographic and thermohaline characteristics. Ca. one third of the OTUs identified in the extracellular DNA were absent from living prokaryotic assemblages, possibly representing the signatures of past assemblages. Our findings expand the knowledge of the contribution of extracellular microbial sequences to current estimates of prokaryotic diversity obtained through the analyses of “environmental DNA”, and open new perspectives for understanding microbial successions in benthic ecosystems.

Highlights

Extracellular DNA in surface deep-sea sediments is by far the largest reservoir of DNA of the world oceans[1]
The concentrations of total extracellular DNA in surface sediments of the continental margins investigated ranged from 9.4 ± 3.0 μg DNA g−1 to 22.5 ± 4.8 μg DNA g−1
Previous studies suggested that the preservation of DNA in deep-sea sediments may be favoured by an array of factors including anoxic conditions, low temperatures, and high sedimentation rates, as observed in continental margins[6,15]

Summary

Introduction

Extracellular DNA in surface deep-sea sediments is by far the largest reservoir of DNA of the world oceans[1]. Previous studies provided evidence that an important fraction of extracellular DNA can escape degradation processes, remaining preserved in the sediments[5,6] This DNA represents, potentially, a genetic repository that records biological processes occurring over time[7,8]. Previous studies suggested that the preservation of DNA might be favoured in benthic systems characterised by high organic matter inputs and sedimentation rates, such as continental margins[15,16] We utilised the extracellular DNA pool as a recorder of the prokaryotic diversity in the sediments of different sites of continental margins (Atlantic and Arctic Ocean, and Mediterranean Sea). The prokaryotic genetic signatures contained in the different extracellular DNA pools were compared among them, www.nature.com/scientificreports/

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