Nitrite-oxidizing bacteria adapted to low-oxygen conditions dominate nitrite oxidation in marine oxygen minimum zones.

Nitrite is a central molecule in the nitrogen cycle because nitrite oxidation to nitrate (an aerobic process) retains fixed nitrogen in a system and its reduction to dinitrogen gas (anaerobic) reduces the fixed nitrogen inventory. Despite its acknowledged requirement for oxygen, nitrite oxidation is observed in oxygen-depleted layers of the ocean's oxygen minimum zones (OMZs), challenging the current understanding of OMZ nitrogen cycling. Previous attempts to determine whether nitrite-oxidizing bacteria in the anoxic layer differ from known nitrite oxidizers in the open ocean were limited by cultivation difficulties and sequencing depth. Here, we construct 31 draft genomes of nitrite-oxidizing bacteria from global OMZs. The distribution of nitrite oxidation rates, abundance and expression of nitrite oxidoreductase genes, and relative abundance of nitrite-oxidizing bacterial draft genomes from the same samples all show peaks in the core of the oxygen-depleted zone (ODZ) and are all highly correlated in depth profiles within the major ocean oxygen minimum zones. The ODZ nitrite oxidizers are not found in the Tara Oceans global dataset (the most complete oxic ocean dataset), and the major nitrite oxidizers found in the oxygenated ocean do not occur in ODZ waters. A pangenomic analysis shows the ODZ nitrite oxidizers have distinct gene clusters compared to oxic nitrite oxidizers and are microaerophilic. These findings all indicate the existence of nitrite oxidizers whose niche is oxygen-deficient seawater. Thus, specialist nitrite-oxidizing bacteria are responsible for fixed nitrogen retention in marine oxygen minimum zones, with implications for control of the ocean's fixed nitrogen inventory.

Partitioning of the denitrification pathway and other nitrite metabolisms within global oxygen deficient zones.

Oxygen deficient zones (ODZs) account for about 30% of total oceanic fixed nitrogen loss via processes including denitrification, a microbially mediated pathway proceeding stepwise from NO3- to N2. This process may be performed entirely by complete denitrifiers capable of all four enzymatic steps, but many organisms possess only partial denitrification pathways, either producing or consuming key intermediates such as the greenhouse gas N2O. Metagenomics and marker gene surveys have revealed a diversity of denitrification genes within ODZs, but whether these genes co-occur within complete or partial denitrifiers and the identities of denitrifying taxa remain open questions. We assemble genomes from metagenomes spanning the ETNP and Arabian Sea, and map these metagenome-assembled genomes (MAGs) to 56 metagenomes from all three major ODZs to reveal the predominance of partial denitrifiers, particularly single-step denitrifiers. We find niche differentiation among nitrogen-cycling organisms, with communities performing each nitrogen transformation distinct in taxonomic identity and motility traits. Our collection of 962 MAGs presents the largest collection of pelagic ODZ microorganisms and reveals a clearer picture of the nitrogen cycling community within this environment.

Blooms of the harmful algae Margalefidinium polykrikoides and Alexandrium monilatum alter the York River Estuary microbiome.

Harmful algal blooms (HABs) cause damage to fisheries, aquaculture, and human health around the globe. However, the impact of HABs on water column microbiomes and biogeochemistry is poorly understood. This study examined the impacts of consecutive blooms of the ichthyotoxic dinoflagellates Margalefidinium polykrikoides and Alexandrium monilatum on the water microbiome in the York River Estuary, Chesapeake Bay, USA. The samples dominated by single dinoflagellate species and by a mix of the two dinoflagellates had different microbiome compositions than the ones with low levels of both species. The M. polykrikoides bloom was co-dominated by Winogradskyella and had increased concentrations of dissolved organic carbon. The A. monilatum bloom had little impact on the prokaryotic portion of the whole community but was associated with a specific group of prokaryotes in the particle-attached (>3 µm) fraction including Candidatus Nitrosopumilus, Candidatus Actinomarina, SAR11 Clade Ia, Candidatus Bealeia, and Rhodobacteraceae HIMB11. Thus, blooms of these two algal species impacted the estuarine microbiome in different ways, likely leading to shifts in estuarine carbon and nutrient cycling, with M. polykrikoides potentially having a greater impact on carbon cycling in the estuarine ecosystem than A. monilatum.

Microbially mediated nitrogen removal and retention in the York River Estuary.

Denitrification, anaerobic ammonium oxidation and dissimilatory nitrate reduction to ammonium (DNRA) are important microbial processes determining the fate of nitrogen (N) in estuaries. This study examined these processes in sediments of the York River Estuary, a tributary of Chesapeake Bay, and investigated environmental and microbial drivers of the rates of denitrification and DNRA. Nitrate reduction followed a consistent pattern throughout the year and across the estuary with nitrogen removal, primarily through denitrification, decreasing from the head of the estuary to the mouth and nitrogen retention, through DNRA, following the opposite pattern. At the mouth of the estuary, nitrogen retention was consistently higher than nitrogen removal. Denitrification rates showed strong linear relationships with concentrations of organic matter, nitrate and chlorophyll a, and the abundance of the nirS gene. DNRA rates were best correlated with the relative abundance of three bacterial families, Anaerolineaceae,Ectothiorhodospiraceae and Prolixibacteraceae, which carry the nrfA gene. The controls responsible for retention or removal of N from an estuary are complex, involving both geochemical and microbial factors. The N retained within estuaries may support primary production and seasonal algae blooms and result in estuarine eutrophication.