Nitrite accumulation and anammox bacterial niche partitioning in Arctic Mid-Ocean Ridge sediments

Abstract

By consuming ammonium and nitrite, anammox bacteria form an important functional guild in nitrogen cycling in many environments, including marine sediments. However, their distribution and impact on the important substrate nitrite has not been well characterized. Here we combined biogeochemical, microbiological, and genomic approaches to study anammox bacteria and other nitrogen cycling groups in two sediment cores retrieved from the Arctic Mid-Ocean Ridge (AMOR). We observed nitrite accumulation in these cores, a phenomenon also recorded at 28 other marine sediment sites and in analogous aquatic environments. The nitrite maximum coincides with reduced abundance of anammox bacteria. Anammox bacterial abundances were at least one order of magnitude higher than those of nitrite reducers and the anammox abundance maxima were detected in the layers above and below the nitrite maximum. Nitrite accumulation in the two AMOR cores co-occurs with a niche partitioning between two anammox bacterial families (Candidatus Bathyanammoxibiaceae and Candidatus Scalinduaceae), likely dependent on ammonium availability. Through reconstructing and comparing the dominant anammox genomes (Ca. Bathyanammoxibius amoris and Ca. Scalindua sediminis), we revealed that Ca. B. amoris has fewer high-affinity ammonium transporters than Ca. S. sediminis and lacks the capacity to access alternative substrates and/or energy sources such as urea and cyanate. These features may restrict Ca. Bathyanammoxibiaceae to conditions of higher ammonium concentrations. These findings improve our understanding about nitrogen cycling in marine sediments by revealing coincident 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.…”

Microbial Niche Differentiation during Nitrite-Dependent Anaerobic Methane Oxidation

“…Since nitrite is usually less abundant in both natural or man-made ecosystems, , whose concentration in environments varies from a few ng L –1 to the mg L –1 level depending on the activities of microbial nitrification and denitrification, , it can also be speculated that the availability of nitrite could be more relevant to the niche differentiation among n-DAMO bacteria and other related microorganisms in anaerobic environments, such as Anammox bacteria. The K m(app) values for nitrite of some Anammox bacteria (such as “ Ca.…”