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1. Non‐denitrifier nitrous oxide reductases dominate marine biomes

   https://doi.org/10.1111/1758-2229.12879  

   Bertagnolli, Anthony D. ; Konstantinidis, Konstantinos T. ; Stewart, Frank J. ( September 2020 , Environmental Microbiology Reports)

   Microbial enzymes often occur as distinct variants that share the same substrate but differ in substrate affinity, sensitivity to environmental conditions, or phylogenetic ancestry. Determining where variants occur in the environment helps identify thresholds that constrain microbial cycling of key chemicals, including the greenhouse gas nitrous oxide (N₂O). To understand the enzymatic basis of N₂O cycling in the ocean, we mined metagenomes to characterize genes encoding bacterial nitrous oxide reductase (NosZ) catalyzing N₂O reduction to N₂. We examined data sets from diverse biomes but focused primarily on those from oxygen minimum zones where N₂O levels are often elevated. With few exceptions, marinenosZdata sets were dominated by ‘atypical’ clade II gene variants. AtypicalnosZhas been associated with low oxygen, enhanced N₂O affinity, and organisms lacking enzymes for complete denitrification, i.e., non‐denitrifiers. AtypicalnosZ often occurred in metagenome‐assembled genomes (MAGs) with nitrate or nitrite respiration genes, although MAGs with genes for complete denitrification were rare. We identified atypicalnosZ in several taxa not previously associated with N₂O consumption, in addition to known N₂O‐associated groups. The data suggest that marine environments generally select for high N₂O‐scavenging ability across diverse taxa and have implications for how N₂O concentration may affect N₂O removal rates.

    

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2. Nitrification and Nitrous Oxide Production in the Offshore Waters of the Eastern Tropical South Pacific

   https://doi.org/10.1029/2020GB006716  

   Santoro, Alyson E. ; Buchwald, Carolyn ; Knapp, Angela N. ; Berelson, William M. ; Capone, Douglas G. ; Casciotti, Karen L. ( February 2021 , Global Biogeochemical Cycles)

   Marine oxygen deficient zones are dynamic areas of microbial nitrogen cycling. Nitrification, the microbial oxidation of ammonia to nitrate, plays multiple roles in the biogeochemistry of these regions, including production of the greenhouse gas nitrous oxide (N₂O). We present here the results of two oceanographic cruises investigating nitrification, nitrifying microorganisms, and N₂O production and distribution from the offshore waters of the Eastern Tropical South Pacific. On each cruise, high‐resolution measurements of ammonium ([NH₄⁺]), nitrite ([NO₂⁻]), and N₂O were combined with¹⁵N tracer‐based determination of ammonia oxidation, nitrite oxidation, nitrate reduction, and N₂O production rates. Depth‐integrated inventories of NH₄⁺and NO₂⁻were positively correlated with one another and with depth‐integrated primary production. Depth‐integrated ammonia oxidation rates were correlated with sinking particulate organic nitrogen flux but not with primary production; ammonia oxidation rates were undetectable in trap‐collected sinking particulate material. Nitrite oxidation rates exceeded ammonia oxidation rates at most mesopelagic depths. We found positive correlations between archaealamoAgenes and ammonia oxidation rates and betweenNitrospina‐like 16S rRNA genes and nitrite oxidation rates. N₂O concentrations in the upper oxycline reached values of >140 nM, even at the western extent of the cruise track, supporting air‐sea fluxes of up to 1.71 μmol m⁻² day⁻¹. Our results suggest that a source of NO₂⁻other than ammonia oxidation may fuel high rates of nitrite oxidation in the offshore Eastern Tropical South Pacific and that air‐sea fluxes of N₂O from this region may be higher than previously estimated.

    

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3. Production and cross-feeding of nitrite within Prochlorococcus populations

   https://doi.org/10.1128/mbio.01236-23  

   Berube, Paul M. ; O'Keefe, Tyler J. ; Rasmussen, Anna ; LeMaster, Trent ; Chisholm, Sallie W. ( July 2023 , mBio)

   Dubilier, Nicole (Ed.)

   Prochlorococcusis an abundant photosynthetic bacterium in the open ocean, where nitrogen (N) often limits phytoplankton growth. In the low-light-adapted LLI clade ofProchlorococcus, nearly all cells can assimilate nitrite (NO₂⁻), with a subset capable of assimilating nitrate (NO₃⁻). LLI cells are maximally abundant near the primary NO₂⁻maximum layer, an oceanographic feature that may, in part, be due to incomplete assimilatory NO₃⁻reduction and subsequent NO₂⁻release by phytoplankton. We hypothesized that someProchlorococcusexhibit incomplete assimilatory NO₃⁻reduction and examined NO₂⁻accumulation in cultures of threeProchlorococcusstrains (MIT0915, MIT0917, and SB) and twoSynechococcusstrains (WH8102 and WH7803). Only MIT0917 and SB accumulated external NO₂⁻during growth on NO₃⁻. Approximately 20–30% of the NO₃⁻transported into the cell by MIT0917 was released as NO₂⁻, with the rest assimilated into biomass. We further observed that co-cultures using NO₃⁻as the sole N source could be established for MIT0917 andProchlorococcusstrain MIT1214 that can assimilate NO₂⁻but not NO₃⁻. In these co-cultures, the NO₂⁻released by MIT0917 is efficiently consumed by its partner strain, MIT1214. Our findings highlight the potential for emergent metabolic partnerships that are mediated by the production and consumption of N cycle intermediates withinProchlorococcuspopulations.

   Earth’s biogeochemical cycles are substantially driven by microorganisms and their interactions. Given that N often limits marine photosynthesis, we investigated the potential for N cross-feeding within populations ofProchlorococcus, the numerically dominant photosynthetic cell in the subtropical open ocean. In laboratory cultures, someProchlorococcuscells release extracellular NO₂⁻during growth on NO₃⁻. In the wild,Prochlorococcuspopulations are composed of multiple functional types, including those that cannot use NO₃⁻but can still assimilate NO₂⁻. We show that metabolic dependencies arise whenProchlorococcusstrains with complementary NO₂⁻production and consumption phenotypes are grown together on NO₃⁻. These findings demonstrate the potential for emergent metabolic partnerships, possibly modulating ocean nutrient gradients, that are mediated by cross-feeding of N cycle intermediates.

    

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4. Diverse nitrogen cycling pathways across a marine oxygen gradient indicate nitrogen loss coupled to chemoautotrophic activity

   https://doi.org/10.1111/1462-2920.15187  

   Suter, Elizabeth A. ; Pachiadaki, Maria G. ; Montes, Enrique ; Edgcomb, Virginia P. ; Scranton, Mary I. ; Taylor, Craig D. ; Taylor, Gordon T. ( August 2020 , Environmental Microbiology)

   Genetic markers and geochemical assays of microbial nitrogen cycling processes, including autotrophic and heterotrophic denitrification, anammox, ammonia oxidation, and nitrite oxidation, were examined across the oxycline, suboxic, and anoxic zones of the Cariaco Basin, Venezuela. Ammonia and nitrite oxidation genes were expressed through the entire gradient. Transcripts associated with autotrophic and heterotrophic denitrifiers were mostly confined to the suboxic zone and below but were also present in particles in the oxycline. Anammox genes and transcripts were detected over a narrow depth range near the bottom of the suboxic zone and coincided with secondary NO₂⁻maxima and available NH₄⁺. Dissolved inorganic nitrogen (DIN) amendment incubations and comparisons between our sampling campaigns suggested that denitrifier activity may be closely coupled with NO₃⁻availability. Expression of denitrification genes at depths of high rates of chemoautotrophic carbon fixation and phylogenetic analyses of nitrogen cycling genes and transcripts indicated a diverse array of denitrifiers, including chemoautotrophs capable of using NO₃⁻to oxidize reduced sulfur species. Thus, results suggest that the Cariaco Basin nitrogen cycle is influenced by autotrophic carbon cycling in addition to organic matter oxidation and anammox.

    

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5. Oxic–anoxic cycling promotes coupling between complex carbon metabolism and denitrification in woodchip bioreactors

   https://doi.org/10.1111/1462-2920.16387  

   McGuire, Philip M. ; Butkevich, Natalie ; Saksena, Aryaman V. ; Walter, M. Todd ; Shapleigh, James P. ; Reid, Matthew C. ( April 2023 , Environmental Microbiology)

   Denitrifying woodchip bioreactors (WBRs) are increasingly used to manage the release of non‐point source nitrogen (N) by stimulating microbial denitrification. Woodchips serve as a renewable organic carbon (C) source, yet the recalcitrance of organic C in lignocellulosic biomass causes many WBRs to be C‐limited. Prior studies have observed that oxic–anoxic cycling increased the mobilization of organic C, increased nitrate (NO₃⁻) removal rates, and attenuated production of nitrous oxide (N₂O). Here, we use multi‐omics approaches and amplicon sequencing of fungal 5.8S‐ITS2 and prokaryotic 16S rRNA genes to elucidate the microbial drivers for enhanced NO₃⁻removal and attenuated N₂O production under redox‐dynamic conditions. Transient oxic periods stimulated the expression of fungal ligninolytic enzymes, increasing the bioavailability of woodchip‐derived C and stimulating the expression of denitrification genes. Nitrous oxide reductase (nosZ) genes were primarily clade II, and the ratio of clade II/clade InosZtranscripts during the oxic–anoxic transition was strongly correlated with the N₂O yield. Analysis of metagenome‐assembled genomes revealed that many of the denitrifying microorganisms also have a genotypic ability to degrade complex polysaccharides like cellulose and hemicellulose, highlighting the adaptation of the WBR microbiome to the ecophysiological niche of the woodchip matrix.

    

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