Comparative genomics sheds light on niche differentiation and the evolutionary history of comammox Nitrospira

Abstract

The description of comammox Nitrospira spp., performing complete ammonia-to-nitrate oxidation, and their co-occurrence with canonical β-proteobacterial ammonia oxidizing bacteria (β-AOB) in the environment, calls into question the metabolic potential of comammox Nitrospira and the evolutionary history of their ammonia oxidation pathway. We report four new comammox Nitrospira genomes, constituting two novel species, and the first comparative genomic analysis on comammox Nitrospira. Unlike canonical Nitrospira, comammox Nitrospira genomes lack genes for assimilatory nitrite reduction, suggesting that they have lost the potential to use external nitrite nitrogen sources. By contrast, compared to canonical Nitrospira, comammox Nitrospira harbor a higher diversity of urea transporters and copper homeostasis genes and lack cyanate hydratase genes. Additionally, the two comammox clades differ in their ammonium uptake systems. Contrary to β-AOB, comammox Nitrospira genomes have single copies of the two central ammonia oxidation pathway operons. Similar to ammonia oxidizing archaea and some oligotrophic AOB strains, they lack genes involved in nitric oxide reduction. Furthermore, comammox Nitrospira genomes encode genes that might allow efficient growth at low oxygen concentrations. Regarding the evolutionary history of comammox Nitrospira, our analyses indicate that several genes belonging to the ammonia oxidation pathway could have been laterally transferred from β-AOB to comammox Nitrospira. We postulate that the absence of comammox genes in other sublineage II Nitrospira genomes is the result of subsequent loss.

Nitrous oxide production by ammonia oxidizers: Physiological diversity, niche differentiation and potential mitigation strategies

“…All comammox bacteria belong to the genus Nitrospira of the class Nitrospira, which also includes canonical nitrite-oxidizing bacteria (Daims, Lücker, & Wagner, 2016), and have been detected in a range of natural and engineered environments (Fowler, Palomo, Dechesne, Mines, & Smets, 2018;Palomo et al, 2018;Pjevac et al, 2017;Wang et al, 2019;Zheng et al, 2019), with the possible exception of oceanic environments. Available amoA gene sequences suggest two phylogenetic groups (clades A and B) of similar diversity with potential environmental specializations.…”

Complete nitrification: insights into the ecophysiology of comammox Nitrospira

“…The general metabolic profiles of strict nitrite-oxidizing and comammox Nitrospira are similar, indicated by the low amount of comammox-specific genes detected by comparative genomics (Palomo et al 2018). Features unique to comammox Nitrospira appear to be mainly the ammonia and hydroxylamine oxidation machinery and the apparent absence of nitrite assimilation and cyanate degradation (Palomo et al 2018).…”

“…N. nitrificans; van Kessel et al 2015) and a biofilm sustained in thermal waters from a 1200-m deep oil exploration well ( N. inopinata ; Daims et al 2015). In addition, analyzing metagenome-assembled genomes (MAGs) of clade B comammox Nitrospira gave first genomic insights into this group so far missing a cultured representative (Orellana et al 2018; Palomo et al 2018). Since the discovery of complete nitrifying Nitrospira , numerous studies have addressed their environmental distribution and abundance (e.g., Bartelme et al 2017; Fowler et al 2018; Hu and He 2017; Orellana et al 2018; Pjevac et al 2017) as well as their potential metabolic capabilities by (meta) genomic analyses (e.g., Camejo et al 2017; Orellana et al 2018; Palomo et al 2016; Palomo et al 2018; Wang et al 2017).…”

Metagenomic recovery of two distinct comammox Nitrospira from the terrestrial subsurface

“…The presence and activity of urease in both canonical and comammox Nitrospira indicate that hydrolysis of urea is a common metabolic feature within this genus (Koch et al, 2015;van Kessel et al, 2015;Ushiki et al, 2018). Intriguingly, while canonical Nitrospira employ a cyanase to utilize cyanate as an additional metabolic source of ammonium (Palatinszky et al, 2015;Ushiki et al, 2018) this function is absent in complete nitrifiers (Palomo et al, 2018).…”

“…The genus Nitrospira, which prior to the discovery of comammox had been regarded to comprise specialized nitrite oxidizers only, represents the most diverse NOB clade, harbouring at least six phylogenetic sublineages observed in a wide range of natural aquatic and terrestrial habitats, and engineered environments like drinking and wastewater treatment plants (Daims et al, 2001;Lebedeva et al, 2011;Daebeler et al, 2014;Daims et al, 2016;Gülay et al, 2016). All complete nitrifiers known to date are affiliated with Nitrospira sublineage II (Daims et al, 2015;van Kessel et al, 2015;Pinto et al, 2016;Palomo et al, 2018). Furthermore, comammox Nitrospira form two divergent clades, referred to as comammox clades A and B, based on phylogenetic analysis of the ammonia monooxygenase (AMO), the enzyme catalysing ammonia oxidation (Daims et al, 2015).…”