Modularity of nitrogen‐oxide reducing soil bacteria: linking phenotype to genotype

Abstract

Model denitrifiers convert NO3- to N , but it appears that a significant fraction of natural populations are truncated, conducting only one or two steps of the pathway. To better understand the diversity of partial denitrifiers in soil and whether discrepancies arise between the presence of known N-oxide reductase genes and phenotypic features, bacteria able to reduce NO3- to NO2- were isolated from soil, N-oxide gas products were measured for eight isolates, and six were genome sequenced. Gas phase analyses revealed that two were complete denitrifiers, which genome sequencing corroborated. The remaining six accumulated NO and N O to varying degrees and genome sequencing of four indicated that two isolates held genes encoding nitrate reductase as the only dissimilatory N-oxide reductase, one contained genes for both nitrate and nitric oxide reductase, and one had nitrate and nitrite reductase. The results demonstrated that N-oxide production was not always predicted by the genetic potential and suggested that partial denitrifiers could be readily isolated among soil bacteria. This supported the hypothesis that each N-oxide reductase could provide a selectable benefit on its own, and therefore, reduction of nitrate to dinitrogen may not be obligatorily linked to complete denitrifiers but instead a consequence of a functionally diverse community.

Metabolic specialization of denitrifiers in permeable sediments controls N2O emissions

“…, Roco et al . , Shapleigh ). The particularly large accumulation of nitrite provided a first indication that nitrate reduction might be mediated by different members of the community than the rest of the pathway in sandy sediments, similar to other environments where nitrate reduction rates are orders of magnitude higher than N 2 production rates (Ganesh et al .…”

“…Such accumulation of denitrification intermediates may have resulted from two factors; 1) poor coupling of individual denitrification steps within single organisms (Bergaust et al, 2008, Lilja and Johnson 2016, Otte et al 1996, Philippot et al 2001 or; 2) process partitioning within the denitrifying community, i.e. the presence of truncated forms of denitrification in different community members (Graf et al 2014, Kuypers et al 2018, Roco et al 2016, Shapleigh 2007. The particularly large accumulation of nitrite provided a first indication that nitrate reduction might be mediated by different members of the community than the rest of the pathway in sandy sediments, similar to other environments where nitrate reduction rates are orders of magnitude higher than N 2 production rates (Ganesh et al 2015, Kalvelage et al 2013.…”

“…Furthermore, each intermediate reaction of the denitrification pathway can occur independently from the others. While denitrification is often studied in model organisms that are 'complete' denitrifiers, it is becoming apparent that a network of N-cycling microorganisms might be responsible for environmental denitrification, with diverse microbes specialized to respire only one or some of the intermediates (Graf et al, 2014, Kuypers et al, 2018, Lilja and Johnson 2016, Philippot et al, 2013, Roco et al, 2016. It has been recognized for many years that some denitrifiers lack a nitrous oxide (N 2 O) reductase (Henry et al 2006, Jones et al 2008, Wood et al 2001.…”

Metagenomic analysis reveals distinct patterns of denitrification gene abundance across soil moisture, nitrate gradients

“…Denitrification is a modular pathway encoded by several functionally redundant genes that is performed by a diverse array of bacteria and archaea (Shapleigh, 2012). Although this pathway represents complete denitrification, the presence of one gene associated with denitrification in a microorganism is not necessarily predictive of the presence of additional genes (Graf et al, 2014;Roco et al, 2016;Lycus, 2017). cNor/qNor, !…”

“…NosZ respectively) to reduce NO 3 − to dinitrogen gas (N 2 ) (Zumft, 1997). Although this pathway represents complete denitrification, the presence of one gene associated with denitrification in a microorganism is not necessarily predictive of the presence of additional genes (Graf et al, 2014;Roco et al, 2016;Lycus, 2017). In order to study the full diversity of denitrifiers, it is therefore necessary to survey all genes in the pathway.…”