Abstract

Marine Bacteroidetes constitute a very abundant bacterioplankton group in the oceans that plays a key role in recycling particulate organic matter and includes several photoheterotrophic members containing proteorhodopsin. Relatively few marine Bacteroidetes species have been described and, moreover, they correspond to cultured isolates, which in most cases do not represent the actual abundant or ecologically relevant microorganisms in the natural environment. In this study, we explored the microdiversity of 98 Single Amplified Genomes (SAGs) retrieved from the surface waters of the underexplored North Indian Ocean, whose most closely related isolate is Kordia algicida OT-1. Using Multi Locus Sequencing Analysis (MLSA) we found no microdiversity in the tested conserved phylogenetic markers (16S rRNA and 23S rRNA genes), the fast-evolving Internal Transcribed Spacer and the functional markers proteorhodopsin and the beta-subunit of RNA polymerase. Furthermore, we carried out a Fragment Recruitment Analysis (FRA) with marine metagenomes to learn about the distribution and dynamics of this microorganism in different locations, depths and size fractions. This analysis indicated that this taxon belongs to the rare biosphere, showing its highest abundance after upwelling-induced phytoplankton blooms and sinking to the deep ocean with large organic matter particles. This uncultured Kordia lineage likely represents a novel Kordia species (Kordia sp. CFSAG39SUR) that contains the proteorhodopsin gene and has a widespread spatial and vertical distribution. The combination of SAGs and MLSA makes a valuable approach to infer putative ecological roles of uncultured abundant microorganisms.

Highlights

  • The phylum Bacteroidetes is the third most abundant group of bacteria in the oceans (Kirchman, 2002) but has been poorly studied at the species level compared to the two other main marine microbial phyla, i.e., Proteobacteria and Cyanobacteria

  • We report the first Multi Locus Sequencing Analysis (MLSA) analysis of the genus Kordia, performed with 98 Single Amplified Genomes (SAGs) from the genus Kordia that were retrieved from a seawater sample from the North Indian Ocean, a location subjected to seasonal monsoon winds and coastal upwelling events as well as open ocean oligotrophy

  • It propagated to the central basin of the Arabian Sea reaching only up to station TARA_039, which was the last mesotrophic station occupied by the Tara Oceans expedition before entering the warm oligotrophic waters of the central basin

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Summary

Introduction

The phylum Bacteroidetes is the third most abundant group of bacteria in the oceans (Kirchman, 2002) but has been poorly studied at the species level compared to the two other main marine microbial phyla, i.e., Proteobacteria and Cyanobacteria. Bacteroidetes is a cosmopolitan phylum that typically constitutes between 4 and 22% of marine bacterioplankton cells (Glöckner et al, 1999; Cottrell and Kirchman, 2000; Alonso-Sáez et al, 2007; Ruiz-González et al, 2012; Lefort and Gasol, 2013; Acinas et al, 2014). Bacteroidetes are proficient at the degradation of particulate organic matter (POM) (Cottrell and Kirchman, 2000; Gómez-Pereira et al, 2012; Fernández-Gómez et al, 2013; Swan et al, 2013) and present a generally high growth rate when substrate is available (e.g., following phytoplankton blooms) (Kirchman, 2002; Ferrera et al, 2011; Buchan et al, 2014). Bacteroidetes can be found in the free-living plankton size fraction, they seem to be predominantly particle-attached (DeLong et al, 1993; Schattenhofer et al, 2009; Crespo et al, 2013; Díez-Vives et al, 2014; Salazar et al, 2015)

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