Viral Metagenomic Content Reflects Seawater Ecological Quality in the Coastal Zone

Anastasia Tsiola,Georgios Kotoulas,Grégoire Michoud,Ioannis Karakassis,Paraskevi Pitta,Daniele Daffonchio,Manolis Tsapakis,Christina Pavloudi,Nomiki Simboura,Stilianos Fodelianakis,Alexandra Pavlidou

doi:10.3390/v12080806

Abstract

Viruses interfere with their host’s metabolism through the expression of auxiliary metabolic genes (AMGs) that, until now, are mostly studied under large physicochemical gradients. Here, we focus on coastal marine ecosystems and we sequence the viral metagenome (virome) of samples with discrete levels of human-driven disturbances. We aim to describe the relevance of viromics with respect to ecological quality status, defined by the classic seawater trophic index (TRIX). Neither viral (family level) nor bacterial (family level, based on 16S rRNA sequencing) community structure correlated with TRIX. AMGs involved in the Calvin and tricarboxylic acid cycles were found at stations with poor ecological quality, supporting viral lysis by modifying the host’s energy supply. AMGs involved in “non-traditional” energy-production pathways (3HP, sulfur oxidation) were found irrespective of ecological quality, highlighting the importance of recognizing the prevalent metabolic paths and their intermediate byproducts. Various AMGs explained the variability between stations with poor vs. good ecological quality. Our study confirms the pivotal role of the virome content in ecosystem functioning, acting as a “pool” of available functions that may be transferred to the hosts. Further, it suggests that AMGs could be used as an ultra-sensitive metric of energy-production pathways with relevance in the vulnerable coastal zone and its ecological quality.

Highlights

Coastal marine ecosystems are frequently under the intense pressure of a wide range of anthropogenic activities, despite their high productivity and provision of goods and services with great socioeconomic imprint [1,2]
Viral community composition at the family level did not differ based on the seawater ecological quality, which was determined by the trophic index (TRIX) range (PERMANOVA, Pseudo-F1,12 = 1.76, p > 0.05)
We found that viral taxonomy did not differ according to the ecological quality of the sampling stations at the family level, rejecting our first hypothesis

Summary

Introduction

Coastal marine ecosystems are frequently under the intense pressure of a wide range of anthropogenic activities, despite their high productivity and provision of goods and services with great socioeconomic imprint [1,2]. Alterations of ecosystem services have been reported due to enrichment with nutrients and organic matter, chemical and biological pollution (i.e., intrusion of heavy metals, hormones, and antibiotics), and other disturbances, which altogether raise concerns about coastal ecosystem sustainability [2]. Within this context, studying the structure of microbial plankton has recently emerged as a complementary approach to characterize ecosystem status (e.g., [3,4]). Marine ecosystem conservation and sustainability are reasonably and tightly linked to prokaryotic diversity and function

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