Distribution and genomic variation of ammonia-oxidizing archaea in abyssal and hadal surface sediments

Ammonia-oxidizing archaea of the phylum Thaumarchaeota play a central role in the biogeochemical cycling of nitrogen in benthic sediments, at the interface between pelagic and subsurface ecosystems. However, our understanding of their niche separation and of the processes controlling their population structure in hadal and abyssal surface sediments is still limited. Here, we reconstructed 47 AOA metagenome-assembled genomes (MAGs) from surface sediments of the Atacama and Kermadec trench systems. They formed deep-sea-specific groups within the family Nitrosopumilaceae and were assigned to six amoA gene-based clades. MAGs from different clades had distinct distribution patterns along oxygen-ammonium counter gradients in surface sediments. At the species level, MAGs thus seemed to form different ecotypes and follow deterministic niche-based distributions. In contrast, intraspecific population structure, defined by patterns of Single Nucleotide Variants (SNV), seemed to reflect more complex contributions of both deterministic and stochastic processes. Firstly, the bathymetric range had a strong effect on population structure, with distinct populations in abyssal plains and hadal trenches. Then, hadal populations were clearly separated by trench system, suggesting a strong isolation-by-topography effect, whereas abyssal populations were rather controlled by sediment depth or geographic distances, depending on the clade considered. Interestingly, genetic variability between samples was lowest in sediment layers where the mean MAG coverage was highest, highlighting the importance of selective pressure linked with each AOA clade’s ecological niche. Overall, our results show that deep-sea AOA genome distributions seem to follow both deterministic and stochastic processes, depending on the genomic variability scale considered.