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Variation in the N isotope effect imparted by ammonium oxidationWhile the ammonium isotope effect, 15ε(NH4+), varies by over 13‰ across all experiments, it exhibits a narrower range for a specific experimental setting with distinct cultivation conditions (mainstream, enrichment, sidestream), it exhibits a broader range across all experiments (Fig. 2). There are a number of possible physiological and experimental conditions that differ among experiments, including reaction rate, temperature, and initial concentration of substrates. As shown in Fig. 6, there is a systematic decrease in 15ε(NH4+) at decreasing initial ammonium concentration, while at the highest ammonium concentrations, the value of 15ε(NH4+) appears to plateau at a value near 32‰, close to the maximum value (32.7 ± 0.7‰) observed by Kobayashi and coworkers in chemostat experiments with enriched cultures19. Typically, the isotope effect imparted into a substrate pool by a kinetic process is set at the first irreversible step; any isotope effects that occur before this point can be expressed, while any that occur after it are concealed37,38. Substrate supply limitations can decrease the reversibility of a given step, and thereby let it modulate the net isotope effect of a multi-step process. This behavior has been proposed to play important roles in controlling the isotopic signatures of microbial sulfate39,40 and nitrate41,42 reduction.Figure 615ε(NH4+) for each individual experiment, compared to the concentration of ammonium at the start of that experiment. Mainstream experiments are plotted in yellow circles, sidestream experiments in blue squares, and enrichment experiments in grey diamonds.Full size imageIn the case of anammox bacteria, this pattern suggests that the relative kinetics of ammonium uptake and oxidation control the observed value of 15ε(NH4+). The typical path of an ammonium molecule through an anammox cell requires crossing several cell membranes to the eventual site of reaction, inside the anammoxosome43,44. When ammonium concentrations are relatively high and ammonium oxidation is not uptake-limited, 15ε(NH4+) is set at the hydrazine synthase (Hzs) enzyme, at which ammonium binds and is subsequently oxidized to hydrazine43. The maximum observed value of 15ε(NH4+) would then be the expression of all isotope effects up to, and including, this bond-breaking step. But if, at relatively low ammonium concentrations in the external medium, the rate of ammonium oxidation is limited by its uptake, then active transport or passive diffusion of ammonium will become the first irreversible step and thereby set the observed value of 15ε(NH4+). Indeed, for assimilatory uptake by a marine bacterium, 15ε(NH4+) has been shown to depend on the external ammonium concentration, varying from 3.8 to 26.5‰ across an ammonium concentration range of 0.3 to 316 mg-N/L, as the first irreversible step changes from active transport at low NH4+ concentrations to diffusion at intermediate concentrations and the enzymatic reaction associated with assimilation at high concentrations18.In the process of NH4+ uptake by anammox bacteria, a number of steps could imaginably impact the isotope effect imparted on the ammonium pool. Prior to oxidation within the anammoxosome, ammonium must cross three membranes to reach the Hzs enzyme44. This is distinct from many other respiratory processes in the N cycle, including aerobic ammonia oxidation, where ammonia is thought to be oxidized in the periplasm45,46. Metagenomic characterization of anammox bacteria in the mainstream system used in these experiments reveals the presence of genes for amt ammonium transporters in these species23, while past studies of Ca. Kuenenia stuttgartiensis shows that anammox bacteria feature a number of genes homologous to those that express AmtB ammonium transporters in other bacteria47,48. These transporters could function to transport ammonium across two membranes, first into the cytoplasm and then into the anammoxosome49. In addition, passive, diffusive influx of ammonium into the cell could play a role, especially at relatively high external ammonium concentrations. Therefore, it is easily imaginable that under different physiological conditions, the observed value of 15ε(NH4+) could reflect (1) free motion of ammonium into the anammoxosome and the full expression of the isotope effect associated with NH4+ oxidation, (2) irreversibility in either of two active transport steps, or (3) irreversibility of diffusive transport of ammonium into the periplasm.We do not know the N isotope effects for ammonium diffusion into the cell and ammonium transport to the anammoxosome. But in analogy to considerations made for the diffusion and active transport of nitrate and active transport into the cells of denitrifying bacteria41, we conclude that it is reasonable to expect the N isotope effects for both passive ammonium diffusion and active transport to be much smaller that the enzyme-level N isotope effect associated with the actual ammonium oxidation. Therefore, when external ammonium is relatively low, and NH4+ transport becomes the rate-limiting step in anaerobic ammonium oxidation, the overall N isotope effect will approach that associated with NH4+ uptake or transport, and will likely be lower than under NH4+-replete conditions, where the full expression of the isotope effect associated with NH4+ oxidation may be expressed. This also supports the observation (Fig. 6) of decreasing 15ε(NH4+) under decreasing ammonium availability.Importantly, in a different microbial setting, e.g., in an oceanic environment, which has anammox bacteria with different (e.g., higher) affinities for ammonium uptake and oxidation, we predict that the same endmember values of 15ε(NH4+) that are seen in these experiments will be observed, but with the relationship between them unfolding at different (e.g., lower) values of ammonium concentration, cell densities, and in turn different cell-specific anammox rates. It is also important to note that the cell-specific anammox rate, not the bulk reaction rate, is the essential parameter for understanding the balance between the different processes at work. Unfortunately, because of the biofilm-dwelling nature of the anammox communities in this study, it is challenging to estimate accurately the number of anammox cells present, and so we were not able to determine the cell-specific anammox rate in our experimental setup. Yet, even at substrate concentrations that are much higher than those typically found in the natural environment, NH4+ uptake can be limiting if the bacterial cell density is high, as is the case in this study.For understanding the role that the balance between ammonium uptake and oxidation may play in controlling 15ε(NH4+), it is useful to compare anammox bacteria to aerobic ammonia oxidizing bacteria (AOB) and archaea (AOA). It is notable that the range of 15ε(NH4+) is similar for anammox bacteria and aerobic ammonia oxidizers; the AOB and AOA express values of 15ε(NH4+) between 14 and 42‰14–17. AOB and AOA perform catabolic ammonia oxidation using the ammonia monooxygenase enzyme. In AOB, this enzyme is located in the periplasm45,46, not in an internal cell structure like the anammoxosome, and so it is unlikely that active transport controls observed isotope effects. Instead, it has been proposed that variations in 15ε(NH4+) for the AOB are related to sequence variations in ammonia monooxygenase16. But recent results from Kobayashi and coworkers suggest that 15ε(NH4+) for anammox bacteria is species-independent; for the three different species tested under similar experimental conditions, the N isotope effects were consistent19. In our experiments, variations in the 15ε(NH4+) values were observed in mainstream and enrichment experiments, where the anammox bacteria population is expected to be similar, which also argues against species dependence. Indeed, the Hzs enzyme seems well conserved across anammox clades50, and, therefore, the ammonium N isotope effect variation observed here cannot be attributed to sequence variations, and is more likely due to the changing experimental conditions (NH4+ concentrations), as discussed above.Irrespective of the explanations for the observed N-isotope effect variability for both ammonium oxidation modes, the overlap in the ranges of values for 15ε(NH4+) for anammox and aerobic ammonia oxidation suggests that in a system that might be either aerobic or anaerobic, the mechanism of ammonium oxidation cannot necessarily be identified based on the ammonium N isotope signature. That is, an enrichment in 15 N associated with ammonium consumption cannot be attributed to ammonia oxidizing bacteria or anammox bacteria based on this measurement alone. Further work to compare the responses of both aerobic ammonia oxidizers and anammox bacteria to changing concentrations and cell-specific reaction rates would be helpful for identifying the overall environmental controls on 15ε(NH4+) under both oxic and anoxic conditions.
15ε(NO2
–) reflects a mixture of processesThe parameter 15ε(NO2–) reflects the weighted sum of the isotope effects for the consumption of nitrite by reduction to N2 and by oxidation to nitrate, and so its value depends on these two processes, as well as upon the stoichiometric ratio between them. For considering the physiology of anammox and its role in a biogeochemical N cycling network, it is of limited use, but in a system where the δ15N of nitrite can be readily measured it is valuable to know how to interpret it. It exhibits relatively little variation across the experimental conditions described here, and is also consistent with the result reported by Brunner and coworkers for Ca. K. stuttgartiensis enrichment cultures (Fig. 3)10, but our results differ from 15ε(NO2–) values for other anammox species by Kobayashi and coworkers19. The principal cause of the constancy of 15ε(NO2–) in these experiments is likely the stability of 15ε(NO2––N2) across all experiments, and is discussed in the sections that follow.The N isotope effect associated with the reduction of nitrite by anammox, 15ε(NO2
––N2), reflects the microbial communityThe N isotope effect associated with the reduction of nitrite to N2 in anammox, 15ε(NO2––N2), is consistent across all three experimental settings (Fig. 5), which is notable when compared to the broad range in 15ε(NO2––N2) observed in previous pure culture experiments with members of the genera Ca. Kuenenia, Ca. Scalindua, Ca. Jettenia, and Ca. Brocadia10,19, as well as in anammox incubation experiments20. This consistancy is also striking in light of the variation of 15ε(NH4+) observed in this study, and suggests that variations in substrate concentrations, reaction rates, or other physiological conditions are not strong controls on 15ε(NO2––N2). Instead, the identity of the anammox bacteria, and in turn its biochemical processing of nitrite, appears to exert control over this isotope effect. In the mainstream system used for these experiments, it has been shown that species in the genus Ca. Brocadia are the principal members of the anammox community present, but that Ca. Kuenenia and Ca. Jettenia are also represented (Table S1)23. Indeed, using the metagenomic characterization of the mainstream system reported by Niederdorfer and coworkers23, as well as the observed values of 15ε(NO2––N2) from previous studies10,19, we calculate an expected value of 15ε(NO2––N2) for the mainstream system of 7.5‰ ± 5.5‰ (1 s.d.). This result is close to, but distinct from, the observed value, and leads to the conclusion that 15ε(NO2––N2) in these systems is the result of a stable mixture of different anammox species, but that the contribution of different species to anammox activity under a specific set of experimental conditions may not directly reflect their cellular abundance. Likewise, although we do not yet know the microbial community composition of the material used in the sidestream experiment, we predict, based on its consistent value for 15ε(NO2––N2), that it is similar to that seen in the mainstream and enrichment settings, and we speculate that this microbial community has been stable over the course of the ~ 5 years between 2014 and 2019.The distinct values of 15ε(NO2––N2) observed for different species can be connected to key variations in the anammox metabolism. Although the canonical anammox mechanism includes the reduction of nitrite to NO by a nitrite reductase enzyme51, genomes of anammox bacteria of the Genus Ca. Brocadia52,53, including 5 of 6 metagenome-assembled genomes for bacteria in the mainstream system used in this study23, typically lack any canonical nitrite reductase in their genomes. Instead, it has been proposed that Ca. Brocadia do not produce NO and instead have hydroxylamine as the intermediate between nitrite and hydrazine52. This hypothesis is supported further by the nature of Hzs, which has two catalytic centers, one of which reduces NO to hydroxylamine, while the second conproportionates hydroxylamine and ammonia to generate hydrazine54; it is possible that Ca. Brocadia can bypass NO entirely and deliver hydroxylamine directly to Hzs.In contrast, Ca. Kuenenia, Ca. Scalindua, and Ca. Jettenia all include a canonical nitrite reductase in their genomes. Indeed, Kobayashi and coworkers19 observed that the offset in 15ε(NO2––N2) between measured values for Ca. Kuenenia and Ca. Scalindua, which have the iron-bearing nitrite reductase NirS, and Ca. Jettenia, which has the copper-bearing nitrite reductase NirK, corresponds to that observed for NirK and NirS in bacterial denitrifiers55. This interpretation is complicated by the observation that the genes for these canonical nitrite reductases are often not expressed49,56 or translated57 under environmental conditions. Nevertheless, the differences in N isotopic discrimination of nitrite among anammox clades appear to correspond to fundamental differences in the conversion of nitrite, but the molecular mechanisms of these steps remain poorly understood.Inverse isotope effect imparted in 15ε(NO2
––NO3
–) by nitrite oxidationA pronounced inverse isotope effect, in which nitrate becomes enriched in 15 N relative to nitrite from which it is produced, was observed in all experimental settings. Such an inverse isotope effect appears to be a signature feature of microbial nitrite oxidation to nitrate, both under oxic and anoxic (i.e., anammox) conditions58,59 In culture-based experiments with nitrite oxidizing bacteria (NOB), 15ε(NO2––NO3–) has been found to vary between − 7.8‰ and − 23.6‰59,60, while anammox bacteria have been shown to express 15ε(NO2––NO3–) values in pure or highly-enriched cultures between − 30 and − 45‰10,19, with values as low as − 78‰ in a wastewater incubation experiment20. In our experiments, we found N isotope effects that cover nearly this whole range (Fig. 4). In both anammox and the NOB, nitrite oxidation is thought to be performed by the enzyme nitrate:nitrite oxidoreductase (Nxr)25,43,59, which is also closely related to bacterial membrane-bound and periplasmic nitrate reductases61,62. The structural details of the Nxr enzyme family are not yet well explored, especially in light of its diverse metabolic roles63, and so it remains unclear what metabolic or microbial processes are responsible for the observed and reported variation in 15ε(NO2––NO3–). At least for anammox bacteria, the inverse kinetic N isotope effect associated with the enzymatic oxidation of nitrite to nitrate may be superposed in part by a relatively large equilibrium N isotope effect between nitrite and nitrate10, perhaps promoted by the reversibility of the enzymatic nitrite oxidation reaction64. It is notable that the most negative end of the observed range for 15ε(NO2––NO3–) in this study approaches the theoretical limit for the isotope effect set by the N isotope equilibrium between nitrite and nitrate, which at 20 °C is – 54.6‰59, and which the NOB have not been observed to approach. This suggests that under the metabolic conditions of anammox, the Nxr enzyme is more likely to catalyze reversible reactions, and so the corresponding N isotope effect is closer to the equilibrium limit, than in aerobic nitrite oxidation. However, the great range observed in 15ε(NO2––NO3–) for anammox makes it difficult to predict a priori how much fractionation anammox will impart on a nitrate pool.On the other hand, observations in this study and elsewhere10,19 (Fig. 4) of values of 15ε(NO2––NO3–) falling near − 30‰ for nitrate generated by anammox match a prediction from water column measurements of N isotope ratios in nitrate and nitrite in the Peru oxygen deficient zone (ODZ)65. The large and variable magnitude of this inverse isotope effect means that even though only ~ 25% of the nitrite oxidized by anammox is converted to nitrate, it can have an outsize effect on nitrate and nitrite pools that can be mistaken for either nitrite oxidation by NOB or nitrite generation by denitrification.Implications for N isotope measurements in natural and engineered environmentsTaken together, the results measured in this study suggest both potential and pitfalls for the application of N isotope measurements to disentangle the systematics of microbial N cycling processes. By its interaction with the nitrate, nitrite, ammonium, and N2 pools, anammox already complicates analysis of the N cycle in any setting where it acts; not only does it impact the stable isotope pools of these molecules, but also its effects on each of these pools can vary greatly depending on physiological or metabolic variables or the identity of the dominant anammox bacteria species. In the context of a wastewater treatment process, measurements of δ15N alone may not be able to directly diagnose what processes are occurring, but when coupled to rate and stoichiometry measurements, may provide insights into the efficiency or limitations of those processes.The removal of 15 N-depleted N by anammox may partly explain the heavy N isotope values ( > 15‰) for nitrate in ODZs that have been formerly attributed to denitrification alone. It remains uncertain, however, what the exact expression of the range of N isotope effects reported here is under natural and variable substrate concentrations. First, as shown here for ammonium, concentration levels will have an effect on the relative kinetics of uptake and oxidation, and in turn on the cell-specific N isotope effect. Second, ammonium concentrations are generally at or below detection in the interior of OMZs, indicating that ammonium supplied by degradation of organic matter may be quantitatively oxidized to N2 by anammox. Under these conditions, the N isotope effect associated with the conversion of ammonium to N2 will be suppressed. Previously published estimates of the overall N isotope effect of dissolved inorganic N (DIN) elimination to N2 in ODZs based on comparing nitrate δ15N values to observed water-column nitrate deficits has inherently included any potential non-fractionating loss of ammonium, and has thus implicitly represented a community N loss isotope effect that depends on the balance between anammox and canonical denitrification. The overall expression on DIN lost by the combined processes of denitrification and anammox in sediments, however, may be completely different. In contrast to nitrate and nitrite66, ammonium is usually not limiting in sediments and its fractional loss to overlying waters allows the N isotope effect of ammonium oxidation to N2 by benthic anammox to be expressed.In both natural and engineered systems where anammox is known to be occurring, measurements of 15ε(NH4+) may be able to diagnose substrate limitations or other physiological limitations. And in the case where ammonium is observed to be consumed by an unknown pathway, it can be expected that isotope effects will fall into a similar range for both aerobic and anaerobic ammonium oxidation; on the other hand, 15ε(NH4+) is of little use for distinguishing ammonium consumption by AOB and anammox. We have also found that despite the great possibility for variation in 15ε(NO2––N2) amongst different anammox species, values of 15ε(NO2––N2) remain relatively stable in a given system that has a stable microbial community, and so this parameter has some potential to be used in monitoring such microbial community stability. Further work is needed to explore how metabolic variation amongst anammox species is related to variations in this parameter, but it appears that subtle changes in the mix of anammox species present, which have no observed effect on anammox rates or stoichiometry can lead to major changes in 15ε(NO2––N2). Finally, this study expands the range of 15ε(NO2––NO3–) for anammox bacteria. On one hand, this result lends further support to the observation that through a strong manifestation of the inverse isotope effect associated with nitrite oxidation, anammox can produce nitrate strongly enriched in 15 N, thereby complicating N mass balances based on tracking the nitrate pool. But we also find that anammox can have 15ε(NO2––NO3–) values much closer to 0‰, falling in the same range as for NOB bacteria, so the contribution of anammox to the δ15N composition of the nitrate pool can in fact vary greatly. Finally, we find that there are no systematic relationships among 15ε(NH4+), 15ε(NO2––N2), 15ε(NO2––NO3–), which is consistent with the conclusion that each of these parameters is controlled at a distinct point in the anammox metabolism. More

High-throughput sequencing resultsA total of 26 million COI reads, 19 million raw 18S V1-V2 reads,, 14 million 18S V4 reads, and 17 million 16S V4–V5 reads were obtained from three Illumina HiSeq runs of amplicon libraries built from pooled triplicate PCRs of 22 environmental samples, 2 extraction blanks, and 4–6 PCR blanks (Supplementary Table S4 online). The in situ pump yielded less raw reads for COI and 16S (Supplementary Fig. S1 online, F = 4.02–14.4, p = 0.0003–0.03), while more raw reads were recovered from both water sampling methods with 18S V4 (F = 6.5, p = 0.007). Water samples generally yielded fewer raw clusters (F = 5.1–35.1, p = 3.2 × 10−6–0.02), except for 18S V4 where numbers were comparable across sample types (Supplementary Fig. S1 online).Bioinformatic processing (quality filtering, error correction, chimera removal, and clustering for metazoans) reduced read numbers to 20 million for COI, 12 million for 18S V1–V2, 11 million for 18S V4, and 10 million for 16S V4–V5, resulting in 10,351 and 17,608 raw OTUs for COI and 18S V1–V2 respectively; 35,538 raw 18S V4 ASVs, and 62,646 raw 16S ASVs (Supplementary Table S4 online). For eukaryote markers, 17–55% of the raw reads remained in PCR blanks after bioinformatic processing, while 50–75% remained in extraction blanks and 52–87% in true samples. In contrast, with 16S, these values were at 87% for PCR blanks, 67% for extraction blanks, and 29–73% for true samples. Thus, negative control samples accounted for 7–13% of bioinformatically processed reads with eukaryotes, compared to 27% with prokaryotes. The vast majority of 16S reads generated by negative controls belonged to a common contaminant of Phusion polymerase kits, which is well amplified in low concentration samples such as negative controls. These reads however accounted for  20 µm size class, and the sampling box targeting both the 2–20 µm and the 0.2–2 µm size classes, detected different community assemblages. For protists, the in situ pump detected higher proportions of ASVs for Bacillariophyta, Ciliophora, Labyrinthulea, or Phaeodarea, while the sampling box detected more cryptophytes, haptophytes, MAST, and telonemians (Fig. 3 18S V4). For prokaryotes, the sampling box detected more diversity in the Alphaproteobacteria, Chloroflexi, or Marinimicrobia (Fig. 3 16S V4–V5). More

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