Research Article: Diversity and relative abundance of ammonia- and nitrite-oxidizing microorganisms in the offshore Namibian hypoxic zone

Date Published: May 21, 2019

Publisher: Public Library of Science

Author(s): Evan Lau, Caitlin H. Frame, E. Joseph Nolan, Frank J. Stewart, Zachary W. Dillard, Daniel P. Lukich, Nicole E. Mihalik, Katelyn E. Yauch, Marcus A. Kinker, Samantha L. Waychoff, Hongbin Liu.

http://doi.org/10.1371/journal.pone.0217136

Abstract

Nitrification, the microbial oxidation of ammonia (NH3) to nitrite (NO2–) and NO2– to nitrate (NO3–), plays a vital role in ocean nitrogen cycling. Characterizing the distribution of nitrifying organisms over environmental gradients can help predict how nitrogen availability may change with shifting ocean conditions, for example, due to loss of dissolved oxygen (O2). We characterized the distribution of nitrifiers at 5 depths spanning the oxic to hypoxic zone of the offshore Benguela upwelling system above the continental slope off Namibia. Based on 16S rRNA gene amplicon sequencing, the proportional abundance of nitrifiers (ammonia and nitrite oxidizers) increased with depth, driven by an increase in ammonia-oxidizing archaea (AOA; Thaumarchaeota) to up to 33% of the community at hypoxic depths where O2 concentrations fell to ~25 μM. The AOA community transitioned from being dominated by a few members at oxic depths to a more even representation of taxa in the hypoxic zone. In comparison, the community of NO2–-oxidizing bacteria (NOB), composed primarily of Nitrospinae, was far less abundant and exhibited higher evenness at all depths. The AOA:NOB ratio declined with depth from 41:1 in the oxic zone to 27:1 under hypoxia, suggesting potential variation in the balance between NO2– production and consumption via nitrification. Indeed, in contrast to prior observations from more O2-depleted sites closer to shore, NO2– did not accumulate at hypoxic depths near this offshore site, potentially due in part to a tightened coupling between AOA and NOB.

Partial Text

Microbial nitrification plays an important role in regulating the availability of nitrogen (N) for biological consumption. In the first step of nitrification, ammonia (NH3) is oxidized to nitrite (NO2−) by ammonia-oxidizing archaea (AOA) or bacteria (AOB), with AOA of the phylum Thaumarchaeota playing a major role in NH3 oxidation in marine systems [1–3]. In the second nitrification step, NO2− is oxidized to nitrate (NO3–) by nitrite-oxidizing bacteria (NOB), with members of the Nitrospina (Nitrospinae), Nitrococcus (Gammaproteobacteria), and Nitrospira (Nitrospirae) among the most common NOB in marine systems [4–8]. The microbes mediating these two steps can be spatially separated or active at different times based on environmental conditions, including the concentrations of inorganic N substrates and dissolved O2 [e.g., 9–11]. Alternatively, AOA/AOB and NOB activity can be tightly coupled, with no NO2− accumulation [e.g., 11,12]. Characterizing the distribution of nitrifying taxa in diverse habitats, such as sites with low dissolved O2 concentrations, can help determine the physical or chemical thresholds that decouple NH3 oxidation from NO2− oxidation, and therefore help predict the accumulation and flux of inorganic N in ocean systems.

Our data from an offshore site in the Benguela Upwelling system identified a prominent nitrifier community whose taxonomic composition varied substantially with depth, and in comparison to prior results from closer to the coast [7]. Consistent with studies showing AOA dominance over AOB in marine systems [1,18,38,65–70], the ammonia oxidizer community at station 116 was composed almost exclusively of Thaumarchaeota (AOA). AOA abundance increased from ~1% at oxic depths to up to 33% in the hypoxic zone, suggesting ammonia as a substantial energy source. In contrast, the NOB community, composed primarily of Nitrospina, never accounted for more than 1% of sequences. However, like the AOA, NOB abundance increased with depth. At depths of peak AOA and NOB abundance, O2 concentrations were low (~20–70 μM) compared to the surface but still considerably higher than levels known to inhibit anaerobic metabolisms such as denitrification and anammox (hundreds of nM to low μM) [e.g., 12,17,79]. Rather, minimum O2 levels at stations 116 and 117 were within the range (tens of μM) known to support high rates of both ammonia and nitrite oxidation within or at the periphery of low-oxygen zones where both AOA and NOB have been found at high abundance [e.g., 7,12–14,36,71,72].

 

Source:

http://doi.org/10.1371/journal.pone.0217136

 

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