Particle-association lifestyle is a phylogenetically conserved trait in bathypelagic prokaryotes

Abstract

The free-living (FL) and particle-attached (PA) marine microbial communities have repeatedly been proved to differ in their diversity and composition in the photic ocean and also recently in the bathypelagic ocean at a global scale. However, although high taxonomic ranks exhibit preferences for a PA or FL mode of life, it remains poorly understood whether two clear lifestyles do exist and how these are distributed across the prokaryotic phylogeny. We studied the FL (<0.8 μm) and PA (0.8–20 μm) prokaryotes at 30 stations distributed worldwide within the bathypelagic oceanic realm (2150–4000 m depth) using high-throughput sequencing of the small subunit ribosomal RNA gene (16S rRNA). A high proportion of the bathypelagic prokaryotes were mostly found either attached to particles or freely in the surrounding water but rarely in both types of environments. In particular, this trait was deeply conserved through their phylogeny, suggesting that the deep-ocean particles and the surrounding water constitute two highly distinct niches and that transitions from one to the other have been rare at an evolutionary timescale. As a consequence, PA and FL communities had clear alpha- and beta-diversity differences that exceeded the global-scale geographical variation. Our study organizes the bathypelagic prokaryotic diversity into a reasonable number of ecologically coherent taxa regarding their association with particles, a first step for understanding which are the microbes responsible for the processing of the dissolved and particulate pools of organic matter that have a very different biogeochemical role in the deep ocean