Abstract

The Amazon River watershed and its associated plume comprise a vast continental and oceanic area. The microbial activities along this continuum contribute substantially to global carbon and nutrient cycling, and yet there is a dearth of information on the diversity, abundance, and possible roles of viruses in this globally important river. The aim of this study was to elucidate the diversity and structure of virus assemblages of the Amazon River-ocean continuum. Environmental viral DNA sequences were obtained for 12 locations along the river's lower reach (n = 5) and plume (n = 7). Sequence assembly yielded 29,358 scaffolds, encoding 82,546 viral proteins, with 15 new complete viral genomes. Despite the spatial connectivity mediated by the river, virome analyses and physical-chemical water parameters clearly distinguished river and plume ecosystems. Bacteriophages were ubiquitous in the continuum and were more abundant in the transition region. Eukaryotic viruses occurred mostly in the river, while the plume had more viruses of autotrophic organisms (Prochlorococcus, Synechococcus) and heterotrophic bacteria (Pelagibacter). The viral families Microviridae and Myoviridae were the most abundant and occurred throughout the continuum. The major functions of the genes in the continuum involved viral structures and life cycles, and viruses from plume locations and Tapajós River showed the highest levels of functional diversity. The distribution patterns of the viral assemblages were defined not only by the occurrence of possible hosts but also by water physical and chemical parameters, especially salinity. The findings presented here help to improve understanding of the possible roles of viruses in the organic matter cycle along the river-ocean continuum. IMPORTANCE The Amazon River forms a vast plume in the Atlantic Ocean that can extend for more than 1,000km. Microbial communities promote a globally relevant carbon sink system in the plume. Despite the importance of viruses for the global carbon cycle, the diversity and the possible roles of viruses in the Amazon are poorly understood. The present work assesses, for the first time, the abundance and diversity of viruses simultaneously in the river and ocean in order to elucidate their possible roles. DNA sequence assembly yielded 29,358 scaffolds, encoding 82,546 viral proteins, with 15 new complete viral genomes from the 12 river and ocean locations. Viral diversity was clearly distinguished by river and ocean. Bacteriophages were the most abundant and occurred throughout the continuum. Viruses that infect eukaryotes were more abundant in the river, whereas phages appeared to have strong control over the host prokaryotic populations in the plume.

Highlights

  • The Amazon River watershed and its associated plume comprise a vast continental and oceanic area

  • Principal-component analysis (PCA) of the physicalchemical data revealed three major groups of samples: river samples, plume samples, and samples from a transition region between them, which is formed by locations near the river mouth

  • Despite the continuum formed by the Amazon River extending from land to ocean, the river and plume represent different ecosystems, characterized by distinct patterns of viral assemblages and water parameters and separated by a transition plume formed by locations St10 and St11

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Summary

Introduction

The Amazon River watershed and its associated plume comprise a vast continental and oceanic area. The microbial activities along this continuum contribute substantially to global carbon and nutrient cycling, and yet there is a dearth of information on the diversity, abundance, and possible roles of viruses in this globally important river. The ocean influences the river, especially during periods of low water levels (November to December) [5, 9,10,11], when the force of ocean tides reverses the river flow near and upstream of the mouth [5, 15] and reduces its level of discharge, an effect that can be detected in the river near the city of Óbidos (Pará state [PA]), which is located 900 km upstream of the river mouth [16] This region between the Óbidos and the river mouth is known as the lower Amazon River. Viral particles can be adsorbed to POM [30] and sink, directly contributing to the deposition of organic matter into the sediment of aquatic systems, or can be advected, contributing to the export of organic matter from river to ocean

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