Abstract
Ammonia-oxidising archaea of the phylum Thaumarchaeota are important organisms in the nitrogen cycle, but the mechanisms driving their radiation into diverse ecosystems remain underexplored. Here, existing thaumarchaeotal genomes are complemented with 12 genomes belonging to the previously under-sampled Nitrososphaerales to investigate the impact of lateral gene transfer (LGT), gene duplication and loss across thaumarchaeotal evolution. We reveal a major role for gene duplication in driving genome expansion subsequent to early LGT. In particular, two large LGT events are identified into Nitrososphaerales and the fate of these gene families is highly lineage-specific, being lost in some descendant lineages, but undergoing extensive duplication in others, suggesting niche-specific roles. Notably, some genes involved in carbohydrate transport or coenzyme metabolism were duplicated, likely facilitating niche specialisation in soils and sediments. Overall, our results suggest that LGT followed by gene duplication drives Nitrososphaerales evolution, highlighting a previously under-appreciated mechanism of genome expansion in archaea.
Highlights
Ammonia-oxidising archaea of the phylum Thaumarchaeota are important organisms in the nitrogen cycle, but the mechanisms driving their radiation into diverse ecosystems remain underexplored
Phylogenomic analysis of 75 concatenated single-copy orthologues retrieved from 152 available thaumarchaeotal genomes (Supplementary Data 1) provided a well-supported thaumarchaeotal phylogenomic tree (Fig. 1), with most nodes with ultrafast bootstrap (UFBoot) values >95% and Shimodaira and Hasegawa-like approximate likelihood ratio test (SH-aLRT) values >95%
Most of the presently available thaumarchaeotal genomes belong to the marine groups, the majority of thaumarchaeotal phylogenetic diversity is present in non-ammonia-oxidising Thaumarchaeota and in ammoniaoxidising archaea (AOA) from terrestrial environments
Summary
Ammonia-oxidising archaea of the phylum Thaumarchaeota are important organisms in the nitrogen cycle, but the mechanisms driving their radiation into diverse ecosystems remain underexplored. We reveal a major role for gene duplication in driving genome expansion subsequent to early LGT. Two large LGT events are identified into Nitrososphaerales and the fate of these gene families is highly lineage-specific, being lost in some descendant lineages, but undergoing extensive duplication in others, suggesting niche-specific roles. Our results suggest that LGT followed by gene duplication drives Nitrososphaerales evolution, highlighting a previously under-appreciated mechanism of genome expansion in archaea. There is currently little evidence for other cases of large lateral gene acquisition in Thaumarchaeota evolution[16,17], and little is known of the relative contributions of gene duplications and genes losses. The aforementioned study only included a limited number of Thaumarchaeota
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