Nitrite accumulation and the associated anammox bacteria niche partitioning in marine sediments

Abstract

By consuming ammonium and nitrite, anammox bacteria form an important functional guild in nitrogen cycling in many environments including marine sediments. Recent studies have shown that anammox bacteria can consume most of the upwardly diffusing ammonium from deep anoxic sediments; however, their impact on the other important substrate nitrite has not been well characterized. Here we show niche partitioning of two anammox families emerges in a 2.4 m long mostly anoxic sediment core retrieved from the Nordic Seas. We document high abundances of anammox bacteria in most investigated sediment layers, with two distinct anammox abundance maxima in two nitrite consumption zones. Between the two anammox abundance maxima, nitrite accumulates as observed in other marine sediment sites and aquatic environments, indicating anammox bacteria play a fundamental role in modulating the nitrite distribution. Anammox bacteria in the upper nitrite consumption zone are dominated by the Candidatus Bathyanammoxibiaceae family, while Ca. Scalinduaceae family dominate at the lower zone. A high-quality representative Ca. Bathyanammoxibiaceae genome is recovered, which, comparing to Ca. Scalindua sediminis, the representative of Scalinduaceae in marine sediments, has fewer high affinity ammonium transporters and lacks the capacity to access alternative substrates or energy sources such as urea and cyanate. These features may restrict Ca. Bathyanammoxibiaceae to conditions of higher ammonium concentrations or fluxes, and therefore drive the observed niche partitioning. These findings improve our understanding about nitrogen cycling in marine sediments by revealing the association between nitrite accumulation and niche partitioning of anammox bacteria.

A new abundant nitrite-oxidizing phylum in oligotrophic marine sediments

“…8B). Such a redox niche preference difference between different lineages of the same functional guild is not novel, but has been previously observed for anammox bacterial families in AMOR sediments 22 . To reflect their preferred redox niches, we propose to name Bin_096 Ca.…”

“…We tested whether the expected AOA to NOB abundance ratio of 6.9:1 is observed in oxic marine sediments by comparing the abundances of AOA and NOB in the oxic zones of 11 sediment cores. The sediment cores considered include eight from the Arctic Mid-Ocean Ridge (AMOR) [four cores reported in 28 , plus GS13-CC2 29 , GS14-GC04 22 , GS14-GC02, and GS15-GC01 30 ], one piston core (NP-U1383E 14,31 ) retrieved from the North Pond of the Mid-Atlantic Ridge, and two piston cores from the North Atlantic Gyre 15 . Oxygen in all but one (GS14-GC04) core penetrates at least 50 cm below the seafloor 14,15,28 .…”

“…2D). All of the marine sites are oligotrophic sediments beneath the oligotrophic gyres of the Pacific 37 , Atlantic 15 , and Indian Oceans 38 , mid-ocean ridges 22,28,30 , hadal trenches 39,40 , and the Gulf of Mexico 41 (Fig. 2C).…”

“…Nitrite rarely accumulates in marine sediments 22,23 , especially in the oxic zone where nitrite is mainly produced by ammonia oxidation. Due to the presence of oxygen, newly produced nitrite is rapidly oxidized to nitrate by NOB.…”

Origin, age, and metabolisms of dominant anammox bacteria in the global oxygen deficient zones

“…Anammox bacteria in the modern ocean are confined within ODZs 46 that occupy only 0.1-1% of the global oceanic volume and are separated by vast oxygenated regions that effectively inhibit the anammox metabolism 47,48 . Instead, given the abundance 37 and relatively high diversity (containing three families) of anammox bacteria in global benthic sediments 20,37,38,49 , we hypothesize that the Scalindua bacteria residing in modern ODZ waters derived from the benthos (Fig. 6).…”