The genome of the ammonia‐oxidizing CandidatusNitrososphaera gargensis: insights into metabolic versatility and environmental adaptations

Abstract

The cohort of the ammonia-oxidizing archaea (AOA) of the phylum Thaumarchaeota is a diverse, widespread and functionally important group of microorganisms in many ecosystems. However, our understanding of their biology is still very rudimentary in part because all available genome sequences of this phylum are from members of the Nitrosopumilus cluster. Here we report on the complete genome sequence of Candidatus Nitrososphaera gargensis obtained from an enrichment culture, representing a different evolutionary lineage of AOA frequently found in high numbers in many terrestrial environments. With its 2.83 Mb the genome is much larger than that of other AOA. The presence of a high number of (active) IS elements/transposases, genomic islands, gene duplications and a complete CRISPR/Cas defence system testifies to its dynamic evolution consistent with low degree of synteny with other thaumarchaeal genomes. As expected, the repertoire of conserved enzymes proposed to be required for archaeal ammonia oxidation is encoded by N. gargensis, but it can also use urea and possibly cyanate as alternative ammonia sources. Furthermore, its carbon metabolism is more flexible at the central pyruvate switch point, encompasses the ability to take up small organic compounds and might even include an oxidative pentose phosphate pathway. Furthermore, we show that thaumarchaeota produce cofactor F420 as well as polyhydroxyalkanoates. Lateral gene transfer from bacteria and euryarchaeota has contributed to the metabolic versatility of N. gargensis. This organisms is well adapted to its niche in a heavy metal-containing thermal spring by encoding a multitude of heavy metal resistance genes, chaperones and mannosylglycerate as compatible solute and has the genetic ability to respond to environmental changes by signal transduction via a large number of two-component systems, by chemotaxis and flagella-mediated motility and possibly even by gas vacuole formation. These findings extend our understanding of thaumarchaeal evolution and physiology and offer many testable hypotheses for future experimental research on these nitrifiers.

Interactions between Thaumarchaea, Nitrospira and methanotrophs modulate autotrophic nitrification in volcanic grassland soil

“…As no cultured AOA has been found to contain more than one copy of the amoA gene (Hallam et al, 2006;Walker et al, 2010;Blainey et al, 2011;Spang et al, 2012) we may assume that copy numbers of archaeal amoA can be directly related to cell abundance. This is not the case for AOB, as several AOB harbor several copies of the amoC/ amoA/amoB gene complex (Chain et al, 2003;Stein et al, 2007;Norton et al, 2008) and it is therefore more reliable to infer AOB cell abundance from 16S rRNA gene quantification.…”

The methanogenic redox cofactor F420 is widely synthesized by aerobic soil bacteria

“…It is thought to serve as the primary catabolic electron carrier in multiple lineages of Euryarchaeota, including representatives of the methanogenic (Eirich et al, 1979), methanotrophic (Michaelis et al, 2002;Knittel et al, 2005) and sulfate-reducing orders (Lin and White, 1986). Genomic and spectroscopic evidence suggests that the cofactor is also synthesized in the aerobic ammonia-oxidizing phylum Thaumarchaeota (Spang et al, 2012). Among bacteria, the cofactor has been chemically identified only within the Actinobacteria, where its physiological roles remain under investigation.…”

Response of ammonia-oxidizing archaea and bacteria to long-term industrial effluent-polluted soils, Gujarat, Western India

“…More recently, genome analysis of Nitrososphaera gargensis revealed that AOA may be adapted to heavy metals containing habitats by encoding multiple metal resistance mechanisms including 21 putative metal ion efflux proteins which belong to 10 different transporter families (Spang et al 2012). Therefore, the reduction of AOA-amoA gene abundance in R2 and R3 soils may not be due to heavy metals alone but also could be attributed to co-contaminated organic pollutants, pH, and higher NH 4 + concentrations.…”

“…Thaumarchaeal "group 1.1b" is shown to participate in ammonia oxidation of strongly acidic soils as well as in heavy metal-contaminated thermal spring (Hatzenpichler et al 2008). Studies indicated that group 1.1b-AOA has the ability to respond to environmental changes by signal transduction via a large number of two-component systems, chemotaxis, and flagellamediated motility (Spang et al 2012). However, laboratory experiments are yet to be done for deciphering metal resistance mechanisms of the group 1.1b-AOA.…”