Microbial niche differentiation explains nitrite oxidation in marine oxygen minimum zones

Abstract

Nitrite is a pivotal component of the marine nitrogen cycle. The fate of nitrite determines the loss or retention of fixed nitrogen, an essential nutrient for all organisms. Loss occurs via anaerobic nitrite reduction to gases during denitrification and anammox, while retention occurs via nitrite oxidation to nitrate. Nitrite oxidation is usually represented in biogeochemical models by one kinetic parameter and one oxygen threshold, below which nitrite oxidation is set to zero. Here we find that the responses of nitrite oxidation to nitrite and oxygen concentrations vary along a redox gradient in a Pacific Ocean oxygen minimum zone, indicating niche differentiation of nitrite-oxidizing assemblages. Notably, we observe the full inhibition of nitrite oxidation by oxygen addition and nitrite oxidation coupled with nitrogen loss in the absence of oxygen consumption in samples collected from anoxic waters. Nitrite-oxidizing bacteria, including novel clades with high relative abundance in anoxic depths, were also detected in the same samples. Mechanisms corresponding to niche differentiation of nitrite-oxidizing bacteria across the redox gradient are considered. Implementing these mechanisms in biogeochemical models has a significant effect on the estimated fixed nitrogen budget.

Constraining the contribution of aerobic nitrite oxidation to oxygen consumption in oceanic oxygen minimum zones

“…In line with earlier work 22,24 , nitrite oxidation rates also declined in response to decreasing DO in most of our experiments (Fig. 4).…”

“…NOB gain energy by oxidizing nitrite to nitrate while using DO as a terminal electron acceptor. NOB appear to have high affinity for DO (K m values of 778-900 nM DO or lower), allowing them to aerobically oxidize nitrite even at nanomolar concentrations of DO 22,24 . Some NOB are also metabolically flexible 25 , and perhaps able to survive anaerobically through the use of alternative electron donors and acceptors 24,26,27 .…”

“…But although in situ nitrite oxidation rates are typically highest under low DO (>100 nmol L -1 d -1 ) [6][7][8][9] , experimental oxygen manipulations show the opposite pattern: declining rates with declining DO 22 . This may be explained by variations in genomic content among different NOB that allow them to occupy distinct, highly-resolved DO niches throughout the water column 4,7,22,24,26 -including those that occur from the edge (20 µM) to the core (<5 nM DO) of OMZs. High DO affinity among some NOB also implies sensitivity to any DO introduced to incubations, and may partly explain some of the elevated rates reported in OMZs.…”

Controls on nitrite oxidation in the upper Southern Ocean: insights from winter kinetics experiments in the Indian sector

“…NO2to NO3by nitrite oxidizing bacteria (NOB), a polyphyletic group of microbes that is not wellunderstood in the ocean (Watson et al, 1986;Beman et al, 2013;Daims et al, 2016;Pachiadaki et al, 2017;Sun et al, 2021). In general, NO2oxidation rate data are limited, with few rate measurements available for the Southern Ocean (Bianchi et al, 1997;Mdutyana et al, 2020;Olson, 1981a).…”

“…Estimates of Km provide information regarding the efficiency of NOB in acquiring substrate NO2 -, with a lower Km indicating a higher affinity for NO2 -, while Vmax denotes the maximum rate of NO2oxidation that can be achieved under a particular set of conditions by a particular NOB community. In the ocean, direct measurements of NO2oxidation kinetic parameters are extremely limited (Olson, 1981;Sun et al, 2017Sun et al, , 2021Zhang et al, 2020), with no estimates available for the Southern Ocean. Km values derived from culture studies of NOB range from 9-544 µM (Nowka et al, 2015;Ushiki et al, 2017), orders of magnitude higher than the existing estimates for natural assemblages of NOB in coastal waters and oxygen deficient zones (ranging from 0.07-0.51 µM; Olson, 1981;Sun et al, 2017;Zhang et al, 2020).…”