Martens-Habbena, W. | bioRxiv Science

bioRxiv2023

Differential substrate affinity and catabolite repression enable preferential use of urea by ammonia-oxidizing bacteria

Four distinct lineages of ammonia-oxidizing microorganisms (AOM) collectively contribute to one of the largest nitrogen fluxes in the global nitrogen budget. AOM possess widely different specific affinities for ammonia, thought to determine their niche differentiation. Nevertheless, ammonia-oxidizing archaea and bacteria (AOA, AOB), and complete ammonia oxidizers (comammox) co-occur in soils, freshwater sediments, and aquifers, suggesting that other factors must drive their coexistence. Here, we show that representatives of four AOM lineages employ distinct regulatory strategies for ammonia or urea utilization, thereby minimizing direct competition for either substrate. The tested AOA and comammox species preferentially used ammonia over urea, while beta-proteobacterial AOB favored urea utilization, repressed ammonia transport in the presence of urea, and showed higher affinity for urea than ammonia, whereas gamma-proteobacterial AOB co-utilized both substrates. Stable isotope tracing, kinetics, and transcriptomics experiments revealed that both assimilation and oxidation of ammonia are transport-dependent. These results reveal novel mechanisms of nitrogen metabolism regulation and transporter-based affinity underlying the contrasting niche adaptation and coexistence patterns among the major AOM lineages.

microbiology↗

bioRxiv2023

A novel order-level lineage of ammonia-oxidizing Thaumarchaeota is widespread in marine and terrestrial environments

Ammonia-oxidizing archaea (AOA) are among the most ubiquitous and abundant groups of Archaea on Earth, widely distributed in marine, terrestrial, and geothermal ecosystems. However, the genomic diversity, biogeography, and evolutionary process of AOA populations in subsurface environments are vastly understudied compared to those of marine and soil AOA. We here report a novel AOA order Candidatus Nitrosomirales that forms a deeply branching basal sister lineage to the thermophilic Ca. Nitrosocaldales. Metagenomic and 16S rRNA gene read mapping demonstrates the dominant presence of Nitrosomirales AOA in various groundwater environments and their widespread distribution across a range of geothermal, terrestrial, and marine habitats. Notably, terrestrial Nitrosomirales AOA show the genetic capacity of using formate as an alternative source of reductant and appear to have acquired key metabolic genes and operons from other mesophilic populations via horizontal gene transfer, including the genes encoding urease, nitrite reductase, and V-type ATPase. Potential metabolic versatility and acquired functions may facilitate their radiation into a variety of subsurface, marine, and soil environments. Molecular thermometer-based evolutionary analysis suggests that Nitrosomirales originated from thermophilic environments and transitioned into temperate habitats in parallel with Nitrososphaerales and Nitrosopumilales. We also provide evidence that terrestrial-marine habitat transitions occurred within each one of the four AOA orders, which reveals a more complex evolutionary trajectory of major AOA lineages than previously proposed. Together, these findings establish a robust taxonomic and evolutionary framework of AOA and provide new insights into the ecology and evolution of this globally abundant functional guild.

microbiology↗