Ecophysiology of uncultivated marine euryarchaea is linked to particulate organic matter

Abstract

Particles in aquatic environments host distinct communities of microbes, yet the evolution of particle-specialized taxa and the extent to which specialized microbial metabolism is associated with particles is largely unexplored. Here, we investigate the hypothesis that a widely distributed and uncultivated microbial group—the marine group II euryarchaea (MGII)—interacts with living and detrital particulate organic matter (POM) in the euphotic zone of the central California Current System. Using fluorescent in situ hybridization, we verified the association of euryarchaea with POM. We further quantified the abundance and distribution of MGII 16 S ribosomal RNA genes in size-fractionated seawater samples and compared MGII functional capacity in metagenomes from the same fractions. The abundance of MGII in free-living and >3 μm fractions decreased with increasing distance from the coast, whereas MGII abundance in the 0.8–3 μm fraction remained constant. At several offshore sites, MGII abundance was highest in particle fractions, indicating that particle-attached MGII can outnumber free-living MGII under oligotrophic conditions. Compared with free-living MGII, the genome content of MGII in particle-associated fractions exhibits an increased capacity for surface adhesion, transcriptional regulation and catabolism of high molecular weight substrates. Moreover, MGII populations in POM fractions are phylogenetically distinct from and more diverse than free-living MGII. Eukaryotic phytoplankton additions stimulated MGII growth in bottle incubations, providing the first MGII net growth rate measurements. These ranged from 0.47 to 0.54 d ⁻¹. However, MGII were not recovered in whole-genome amplifications of flow-sorted picoeukaryotic phytoplankton and heterotrophic nanoflagellates, suggesting that MGII in particle fractions are not physically attached to living POM. Collectively, our results support a linkage between MGII ecophysiology and POM, implying that marine archaea have a role in elemental cycling through interactions with particles.