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OBITUARY
15 October 2020

Pioneer of biodiversity accounting who overhauled the Red List of threatened species.

Nathalie Pettorelli

Nathalie Pettorelli, a senior research fellow, started at the Institute of Zoology, London under Georgina’s directorship; they co-supervised a PhD student at Imperial College London.
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Credit: Jussi Puikkonen/KNAW

Georgina Mace shaped two cornerstones of modern ecology and conservation. One was the global inventory of species threatened with extinction, the International Union for Conservation of Nature (IUCN) Red List. The second was the United Nations Millennium Ecosystem Assessment. One of the sharpest minds of her generation, she strove to document and stem biodiversity loss with analytical rigour and multidisciplinary approaches. She died on 19 September, aged 67.
Throughout her career, Mace developed tools for evidence-based policymaking. Before her, the Red List was based on nominations from experts rather than data, undermining confidence in its accuracy. She devised criteria to standardize assessments. The Red List is now the most used and trusted source for assessing trends in global biodiversity.
Mace was born in London in 1953. She studied zoology at the University of Liverpool, UK, before doing a PhD in the 1970s at the University of Sussex in Brighton, UK, where John Maynard Smith was pioneering mathematical approaches to evolutionary ecology. As a postdoc at the Smithsonian Institution in Washington DC, she studied the impacts of inbreeding on captive animals.
In 1983, she joined the Institute of Zoology, the research arm of the Zoological Society of London, where she remained for 23 years, latterly as director from 2000 to 2006. There, Mace continued to work on the genetic management of zoological collections and small populations. Her findings informed the conservation status of several species, including the western lowland gorilla (Gorilla gorilla gorilla), and highlighted the value of reproductive technology in managing captive populations of endangered species, such as the Arabian oryx (Oryx leucoryx) and Przewalski’s horse (Equus przewalskii). She became increasingly interested in population viability, extinction risk and setting conservation priorities.
In 1991, this led her, together with US population biologist Russell Lande, to question the IUCN categories of threats and the associated nomination process as being largely subjective. They suggested three categories: critical, endangered and vulnerable. These they defined in terms of the probability of a species becoming extinct within a specific period, such as five years or two generations. They drew up standardized criteria based on population-biology theory. These included, for example, total effective population size, the population trend over the past five years and observed or projected habitat loss. Mace later introduced, among other things, categories for species that are not currently under threat. This work ultimately defined the categories that the IUCN uses now.
In 2006, Mace became director of the NERC Centre for Population Biology at Imperial College London. There, she worked on the definition of biodiversity targets and assessing species’ vulnerability to climate change. She also studied the link between biodiversity and ecosystem services — the benefits that humans draw from nature, such as carbon sequestration, medicines or waste decomposition.
From 2012, as founding director of the Centre for Biodiversity and Environment Research at University College London, she developed an interest in natural-capital accounting, the process of calculating the total stocks and flows of natural resources and services in an ecosystem or region. Her blending of economics and ecological theory to define a risk register for natural capital helped to provide an effective focus for monitoring and data gathering. It also contributed to a common understanding of priorities across fields.
Mace bridged the gaps between genetics, population ecology and macroecology, sub-disciplines in which she regularly supervised students, networked and published. She also demonstrated the importance of conservationists engaging with researchers in other disciplines, such as climate science, economics and social science. She excelled in building consensus, a key step towards evidence-based policy.
Mace was coordinating lead author for biodiversity on the Millennium Ecosystem Assessment, launched in 2001, which demonstrated that rapidly growing demand for food, fresh water, timber, fibre and fuel resulted in a large and largely irreversible loss in biodiversity. She supported the development of assessments for the biodiversity target of the UN Convention on Biological Diversity in 2010 and, most recently, acted as review editor for the Global Assessment of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. She held similarly pivotal roles at the national level, on UK climate and environmental assessments.
She broke several glass ceilings. Mace was the first president of the international Society for Conservation Biology from outside North America, and the first female president of the British Ecological Society. Her many awards and honours included a fellowship of the Royal Society and, in 2016, she was made a dame.
Georgina was a role model: firm but fair, collaborative, reliable, unassuming, approachable — the kind of critical friend we all need. She supported the career progression of numerous ecologists and influenced many more. She’d nominate you for a post even when you didn’t think she had noticed your work; she’d make a witty remark in the middle of a heated discussion. Few knew that she had cancer. Never one to make a fuss about herself, nine days before she died, she published a paper on habitat conversion and biodiversity loss (D. Leclère et al. Nature 585, 551–556; 2020). Her death leaves a void: she will be sorely missed.

Nature 586, 495 (2020)

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Effects of FeS on nitrogen removal
The start-up period could be divided into two phases based on the operating strategy of the reactor, as illustrated in Table 1. The first phase was characterized by high HRT and low substrate concentration (days 0–18), in which the HRT was 48 h and the concentrations of influent NH4+-N and NO2−-N were 50 and 60 mg L−1, respectively. The second phase was characterized by low HRT and high substrate concentration (days 24–68), in which the HRT was 36 h and the theoretical concentrations of influent NH4+-N and NO2−-N were 100 and 120 mg L−1, respectively.
Table 1 Operational conditions of R1 and R2 under different phases.
Full size table

The effluent ammonium concentration was significantly higher than that of influent at the beginning of the reactor operation shown in Fig. 1a. On the first day, the effluent NH4+-N concentration of R1 and R2 reached 106.0 and 80.6 mg L−1, respectively, nearly twice as high as the influent NH4+-N concentration. This is mainly due to the fact that some microorganisms were unable to adapt to the new environmental conditions, inducing cellular lysis21. At the same time, effluent NO2−-N concentration of R1 and R2 on the fourth day were 18.4 and 17.3 mg L−1, respectively, with the removal efficiency of more than 70% (Fig. 1b); and NO3−-N accumulated in the effluent. The high-throughput results showed that Nitrospirae, which contained massive nitrite-oxidizing bacteria (NOB), accounted for a higher proportion in the inoculation sludge (Supplementary Fig. 1)22. qPCR results also indicated that NOB abundance was higher in the inoculation sludge as shown in the section “Effect of FeS on functional bacteria abundance”. Therefore, the removal of NO2−-N in the beginning might be attributed to the role of nitrification. Denitrification also might promote the decrease of NO2−-N through using the organic matter which was released by decay of biomass23. From day 7 to day 10, effluent NH4+-N of R1 and R2 decreased rapidly from 38.1 and 49.4 mg L−1 to 6.8 and 6.8 mg L−1, respectively, however the removal rate of NO2−-N did not change much. From day 1 to day 18, the accumulation of NO3−-N in R1 and R2 gradually decreased from 10 mg L−1 to 0 mg L−1. These phenomena indicated that NOB was gradually eliminated in the low-oxygen environment and the activity of anammox bacteria was increasing. In addition, microbial metabolism and decay of biomass will release organic carbon, which can be used as carbon sources by denitrifying bacteria23. From day 4 to day 18, the total nitrogen removal efficiency (TNRE) of R1 and R2 increased from 30.4% and 22.2% to 96.0% and 98.3%, respectively. On day 18, the values of removed NO2−-N/NH4+-N and produced NO3−-N/removed NH4+-N were 1.14 and 0 in R1 while these were 1.17 and 0 in R2, which was the result of the combined action of nitrifying bacteria, denitrifying bacteria and anammox bacteria.
Fig. 1: Nitrogen removal performances of R1 and R2.

a Influent and effluent NH4+-N concentration; b Influent and effluent NO2−-N concentration; c Nitrogen loading rate (NLR), nitrogen removal rate (NRR), and total nitrogen removal efficiency (TNRE).

Full size image

On the 21st day, when influent NH4+-N and NO2−-N concentrations increased to 100.3 and 138.1 mg L−1, effluent NH4+-N and NO2−-N concentrations of R1 increased to 6.5 and 24.2 mg L−1, respectively; while those of R2 increased to 2.6 and 19.9 mg L−1. On the 24th day, when HRT decreased from 48 h to 36 h, effluent NH4+-N and NO2−-N continued to increase. At this time, the abundance of anammox bacteria in the reactors was relatively low and had not played a dominant role. Meanwhile, the cell lysis phase was over and denitrifying bacteria activity began to decrease with the continuous consumption of organic substance23. Therefore, the NH4+-N and NO2−-N removal efficiencies fluctuated widely when the nitrogen loading rate (NLR) increased. Moreover, the higher removal rate of NH4+-N and NO2−-N in R2 can be attributed to the promotion effect of FeS on anammox growth. On the 27th day, effluent NO2−-N concentration of R1 and R2 reached the highest values (81.8 mg L−1, 71.1 mg L−1); the TNRE was the lowest, which were 52.8% and 61.0%, respectively. After this point, the NH4+-N and NO2−-N removal efficiencies of both R1 and R2 gradually increased and there were significant differences in total nitrogen removal capability between the two reactors. As shown in Fig. 1c, the TNRE of R2 on the 30th day increased to 73.3%; R1 achieved a TNRE of over 70% 12 days later, while the TNRE of R2 reached over 80% at this time. On the 45th day, the accumulation of nitrate appeared again in the effluent of the two reactors, meaning anammox was predominant. On the 51st day, the NH4+-N and NO2−-N removal in R2 reached more than 85% simultaneously, and the values of removed NO2−-N/NH4+-N and produced NO3−-N/removed NH4+-N were 1.12 and 0.17, respectively, closing to the theoretical stoichiometric ratio of anammox reaction, which marks that anammox reactor was started up successfully21. Based on Eq. (1) and the experimental data on day 51, an assumed transformation model was constructed to reflect the pathways of the nitrogen conversions in the system as shown in Supplementary Fig. 2. Due to the lack of oxygen and organic matter and the inhibition of denitrification by FeS, anammox played a dominant role. The same phenomenon occurred in R1 on day 56. Bi et al. studied the effect of Fe(II) concentration on the start-up of anammox process with a HRT of 12 h and found that the start-up time of anammox process could be shortened from 70 to 58 days when the concentration of Fe(II) ranged from 1.68 to 3.36 mg L−121. Because the concentration of Fe(II) was relatively lower than previous study, the influence was relatively less but this method is more convenient. The heme c content at day 50 in R2 was higher than that in R1 as shown in the section “Fe2+ release and Heme c content”, demonstrating that the activity of anammox bacteria in R2 was higher than that in R1. In summary, FeS effectively shortened the start-up time and improved the nitrogen removal performance.
On the 71st day, when influent NH4+-N and NO2−-N concentrations increased to 150 mg L−1 and 180 mg L−1, respectively, the NH4+-N and NO2−-N removal rates in the two reactors decreased. On the 75th day, effluent NH4+-N concentrations of R1 and R2 increased to 37.1 and 35.3 mg L−1, meantime effluent NO2−-N concentration increased to 93.3 and 84.8 mg L−1. Although the nitrogen removal rate of the two reactors decreased obviously after the NLR was increased, it quickly recovered to the original level. As shown in Fig. 1a, b, on day 81, effluent NH4+-N in R1 and R2 decreased to 11.1 and 7.1 mg L−1 and effluent NO2−-N concentrations decreased to 16.5 and 6.2 mg L−1. The TNRE increased to about 90%. This indicated that the reactors have a certain capacity in resistance to weak shock loading due to the enrichment of anammox bacteria. And, when influent NH4+-N and NO2−-N were further increased, effluent NH4+-N and NO2−-N concentrations of R2 were significantly lower than these of R1. Meantime, the responses caused by the unit intensity of shock (R) of R2 was substantially lower than these of R1 as shown in Supplementary Table 1, indicating that R2 had more resistance to shock loading rate. The same trend was observed when HRT were further shortened to 36 h and 12 h, suggested that the stability of anammox reactors can be improved with the addition of FeS.
During the start-up period, the NO3−-N concentration in R2 was substantially higher than that in R1 as shown in Supplementary Fig. 3, which might be attributed to the inhibition of denitrification process in R2 by FeS24,25. However, in the stabilization period, the NO3−-N concentration in R2 was substantially lower than that in R1. This was due to the lack of organic matter in R1 which inactivated denitrifying bacteria. Meantime, the presence of FeS in R2 might promote sulfur autotrophic denitrification and DNRA to reduce nitrate. The KEGG function prediction result as shown in the section “Effect of FeS on microbial community” verified this inference.
FeS structure change
The appearance of FeS with dark brown color, particle size between 1 and 5 mm and compact texture before being added to the reactor was observed (Supplementary Fig. 4). After 180 days of reactor operation, the FeS materials remaining in R2 were found to be covered with a layer of sludge. And the appearance displayed clear differences: most of the color changed from dark brown to khaki and the texture was sparse, which may be caused by the oxidation of FeS. Moreover, the red anammox granule sludge as shown in Supplementary Fig. 4 was observed in R2. Touching these red anammox granule sludge felt that the interior was relatively hard, which was made of FeS particles. FeS may promote the formation of anammox granular sludge.
To further understand the structure change, the morphology of FeS before and after reaction were observed by SEM at different magnifications. As shown in Fig. 2c, d, there were many honeycomb style holes on the surface and inside of the FeS particles after the reaction. The voids formed on the surface may facilitate the attachment of microorganisms, which acted like microbial carriers. Therefore, anammox granular sludge containing FeS as inert cores formed in R2. In addition, Fe2+/Fe3+ produced by oxidation and ionization of FeS could weaken the electrostatic repulsion among negatively charged anammox cells and promote the aggregation of anammox bacteria into zoogloea by the effect of salt bridge26. Thus, the addition of FeS could promote the formation of anammox granular sludge, then improve the stability of the reactor. Figure 2e, f showed that many plate-shaped secondary minerals were produced after the reaction of FeS. In the presence of dissolved oxygen (DO), O2 can diffuse into the FeS surface and oxidize Fe2+ to Fe3+ (Eq. (5))6. The formation of these secondary minerals may hinder the release of iron ions from FeS27.

$${mathrm{FeS}} + {mathrm{2}}{mathrm{.25}}{mathrm{O}}_2 + {mathrm{2}}{mathrm{.5}},{mathrm{H}}_2{mathrm{O}} to {mathrm{Fe}}({mathrm{OH}})_3 + {mathrm{S}}{mathrm{O}}_4^{{mathrm{2}} – } + {mathrm{2}}{mathrm{H}}^ +$$
(5)

Fig. 2: SEM of FeS.

Before (a, b) and after (c–f) reaction.

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Effect of FeS on functional bacteria abundance
The abundance of anammox bacteria in the two reactors were monitored during the period of their operation. As shown in Fig. 3a, the copy numbers of anammox 16S rRNA gene in the inoculation sludge was 3.31 × 106 copies per ng DNA. After 150 days of cultivation, the copy numbers of anammox 16S rRNA gene in R1 and R2 (1.21 × 107, 1.42 × 107copies per ng DNA) were significantly higher than that in the inoculation sludge. The data demonstrate that although the content of anammox in the inoculation sludge was low, anammox bacteria can be rapidly enriched and the reactor could be properly started-up as long as the cultural conditions for anammox bacteria growth were suitable. The anammox 16S rRNA gene copy numbers of R1 and R2 were 5.68 × 106 and 7.04 × 106 copies per ng DNA on day 70, respectively. Compared with R1, the abundance of anammox bacteria in R2 was increased by 29%. The contrast in cell quantities between R1 and R2 indicated that the addition of FeS with this concentration promoted the growth of anammox bacteria. Combined with the water quality results, the faster growth rate of anammox bacteria in R2 was responsible for the higher removal efficiencies of NH4+-N and NO2−-N and shorter start-up time of reactor.
Fig. 3: The qPCR results of sludge samples.

a Anammox 16S rRNA gene copy number in different period; b other functional genes copy number on day 70. Data indicate average, and error bars represent standard deviation of the results from three independent sampling, each tested in triplicate.

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In addition to anammox, the contents of ammonia-oxidizing bacteria (AOB), NOB and denitrifying bacteria also affect the start-up time and nitrogen removal capacity of anammox reactor. Compared with the inoculation sludge, the expression levels of amoA (NH4+ → NO2−) and nirS (NO3− → NO2−) genes in both R1 and R2 were increased, while the expression levels of Nitrospira spp. 16S rRNA genes (NO2− → NO3−) and nirK (NO3− → NO2−) genes were decreased (Fig. 3b). The expression levels of Nitrospira spp. 16S rRNA genes could reflect the content of NOB in anammox reactor28. As anammox was cultured in an anaerobic environment, which was not conducive to the growth of NOB, the content of NOB was gradually decreased with the increase of culture time. And the expression level of Nitrospira spp. 16S rRNA genes in the inoculated sludge was 2.14 × 106 copies per ng DNA, which was consistent with the higher nitrite removal efficiency initially. On day 70, the expression levels of amoA gene in R1 and R2 were 1.34 × 104 and 2.07 × 103 copies per ng DNA, while anammox 16S rRNA gene expression level was 5.68 × 106 and 7.04 × 106 copies per ng DNA. It was clear that the content of anammox was two or three orders of magnitude higher than AOB. The qPCR results also demonstrated that the anammox bacteria were dominant after 70 days of operation, at which time the removal of ammonium nitrogen was mainly from anammox. In addition, the expression level of amoA gene in R2 was much lower than that of R1, and the NOB content of both reactors was higher than AOB content on day 70 (Fig. 3b). FeS could react with dissolved oxygen (DO) in the reactor, leading to an inhibitory effect on the growth of AOB6. But Nitrospira-like NOB has higher hypoxia tolerance ability than AOB. Liu et al. reported that when the reactor was operated under low oxygen conditions (0.16 mg DO L−1) for a long time, some of Nitrospira-like NOB can adapt to anaerobic environment and maintain activity29. Both nirS and nirK are functional genes of denitrifying bacteria. The expression level of nirS gene in R2 (2.05 × 106 copies per ng DNA) was higher than that of R1 (1.11 × 106 copies per ng DNA), while the expression of nirK gene in R2 (3.27 × 106 copies per ng DNA) was slightly lower than that of R1 (3.65 × 106 copies per ng DNA). According to previous reports, the nirK gene encodes copper-containing nitrite reductase and the nirS gene encodes heme-containing cd1 nitrite reductase which contains heme d as its catalytic center30. And iron ions are involved in the synthesis of various types of heme. It is reasonable to speculate that the synthesis of cd1 nitrite reductase in microorganisms was promoted after adding FeS into the reactor.
Fe2+ release and Heme c content
The effluent Fe2+ and intracellular heme c concentrations were determined and illustrated in Fig. 4. Initially, the Fe2+ content in the effluent of R1 and R2 was similar because FeS particles with compact texture had a smaller specific surface area (Fig. 2a, b) and released less iron ions (Fig. 4a). After the reactor was operated for a period, the effluent Fe2+ concentration of R2 was significantly higher than that of R1. On the 30th day, the effluent Fe2+ concentration of R1 and R2 were 0.132 and 1.762 mg L−1, respectively. The results on days 45 and 60 also showed that there was a significant difference in effluent Fe2+ concentration between R1 and R2. During this period, massive holes were corroded on the surface and inside of FeS particles as shown in Fig. 2, the specific surface area of FeS increased and the activity of FeS was higher, contributing to more release of iron ions. On day 70, the content of heme c in R1 and R2 was 7.2 and 11.8 μmol per g-protein, respectively (Fig. 4b). It has been reported that Fe2+ was involved in the formation of heme c, which was the active center of many enzyme proteins31. In many biochemical reactions, the transformation of substrate and intermediate is accomplished by the catalysis and electron transfer of c-type heme protein32,33. Anammox cells contain a large amount of multi-heme cytochromes, for example one subunit of hydroxylamine oxidoreductase enzyme (HAO) binds 8 heme c34. In this experiment, the positive correlation between Fe2+ and heme c confirmed that the concentration of Fe2+ in the reactor could be increased with the addition of FeS, then promoting the synthesis of heme c. On the 75th and 90th days, the Fe2+ content in the effluent of both reactors became lower, probably because the abundance of anammox bacteria increased gradually, corresponding to an increased consumption of iron ions. At the same time, the results showed that the content of Fe2+ in R2 effluent did not differ much from that in R1 effluent. On one hand, as the reaction progress, secondary minerals and biofilm were formed on the surface of FeS (Fig. 2), which led to a decrease in FeS activity. On the other hand, the abundance of anammox bacteria in R2 was higher than that in R1 (Fig. 3), thus more iron ions would be consumed.
Fig. 4: Effluent Fe2+ concentration and the content of Heme c.

a effluent Fe2+ concentration; b the content of Heme c. Data indicate average, and error bars represent standard deviation of the results from three independent sampling, each tested in triplicate.

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Effect of FeS on microbial community
Through clustering analysis of OTU, the number of OTUs shared among samples and the number of OTUs unique to each sample can be intuitively observed. The number of OTUs shared by the R1 and R2 samples was 816, which accounted for 71.8% and 69.9% of the total OTUs, respectively; the number of OUT unique to R1 was 321 and that for R2 was 352 (Supplementary Fig. 5). The addition of FeS led to different species composition of the two communities. The shared OTUs number of R1 and R2 samples with inoculated sludge was 168, accounting for 14.8% and 14.4% of the total OTUs of R1 and R2 samples, respectively. Obviously, after domestication, the R1 and R2 samples were less similar to the inoculated sludge.
The ACE, Chao1, Simpson and Shannon listed in Table 2 are the alpha diversity indexes that reflect the richness and diversity of the community. The ACE and Chao 1 indexes are mainly used to indicate the richness of the community. In general, the larger the two index values are, the higher the richness of the community is. Comparing the ACE and Chao1 index values of R1 and R2 samples, the richness of R2 community was higher than that of R1. The Simpson and Shannon indexes account for the richness and evenness of the community. The larger the two index values are, the higher the diversity of the community is. As shown in Table 2, the two index values of R2 samples were higher than these of R1, so the diversity of R2 community was higher. In summary, the community of R2 sample had higher richness and diversity. During the cultivation and acclimation process, some species in the seed sludge couldn’t adapt to the new environmental conditions and were gradually washed out from the system. The addition of FeS reduced the tendency of some species to disappear under its role in facilitating the formation of granular sludge.
Table 2 The OTU numbers and bacterial diversity indices of sludge samples.
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It can be seen from the results of microbial diversity analysis that the addition of FeS had a certain influence on the number of species of R1 and R2. The differences in microbial community composition at different classification levels with or without the presence of FeS were shown in Fig. 5.
Fig. 5: The microbial community of sludge samples at different levels on day 180.

a Phylum level; b top 9 abundant genera at genus level; c the microbial community of Brocadiaceae.

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The microbial community composition of R1 and R2 was similar at phylum classification level (Fig. 5a). The dominant phylum in two reactors was Protobacteria, accounting for 40.1% and 29.6%, respectively, followed by Chloroflexi (12.5% and 14.1%). Other reports also showed there were higher contents of Protobacteria and Chloroflexi in anammox reactor35,36. The relative abundance of Planctomycetes which anammox belonged to in R1 and R2 was 9.1% and 9.9%, respectively. The values were not very high, mainly due to the small proportion of Planctomycetes in the inoculated sludge (Supplementary Fig. 1) and the slower growth rate of the anammox bacteria. The proportion of Acidobacteria in R1 and R2 showed obvious difference, with relative abundances of 7.0% and 11.9%, respectively. Several publications demonstrated that some microorganisms belonged to Acidobacteria have the ability to dissimilate iron reduction with various simple organic acids such as acetate as alternative electron donors under anaerobic conditions37,38,39. In addition, the relative abundance of Nitrospirae which Nitrospira belonged to in R1 and R2 was extremely low compared with the inoculated sludge, which was reduced from 16.58% to 0.45% and 0.15%, respectively (Supplementary Fig. 1). This result was consistent with the water quality.
Figure 5b showed the genus of the top 9 abundance in the microbial community of R1 and R2. The most abundant genus in R1 was Halomonas, accounting for 9.7%. Most parts of the microbes belonged to Halomonas were denitrifying bacteria, which could reduce NO3−-N to NO2−-N40. Denitratisoma with a high relative abundance (7.3%) in R1 is also one type of denitrifying bacteria41. The proportions of Halomonas and Denitratisoma in R2 was 6.5% and 4.3%, respectively, significantly lower than these in R1. The relative abundance of Thiobacillus, which was the major autotrophic denitrifier detected in most sulfur-based autotrophic denitrification reactors, increased from 0.012% in R1 to 0.041% in R2 with the addition of FeS42,43. The most abundant genus in R2 was Clone_Anammox_20, accounting for 9.0%. Clone_Anammox_20 and Clone_Anammox_2 are a class of microorganisms with anammox function. The most abundant anammox genus obtained in both reactors was “Ca. Kuenenia” and the proportion was relatively close. In order to further explore the effect of FeS on the distribution of anammox bacteria, the composition of R1 and R2 samples on Brocadiaceae classification level was analyzed. The Brocadiaceae family in R1 consisted of three anammox genus, “Ca. Kuenenia”, “Ca. Brocadia” and “Ca. Jettenia”, accounting for 99%, 0.9%, and 0.1%, while the Brocadiaceae family in R2 consisted of two anammox genus, “Ca. Kuenenia” and “Ca. Brocadia”, accounting for 98% and 2%, respectively (Fig. 5c). The dominant anammox bacteria in R1 and R2 was “Ca. Kuenenia”, and the proportion of “Ca. Brocadia” in R2 was higher than in R1. Other works have found that some of the anammox bacteria under the genus “Ca. Kuenenia” and “Ca. Brocadia” could oxidize Fe2+ with NO3−-N while anammox process occurred44. Thus, FeS might affect the distribution of species and relative abundance of anammox genus but did not change the dominant status of the anammox bacteria in the community.
To further explore the influence mechanism of FeS on nitrogen transportation, PICRUSTs was used in this experiment to predict the contents of enzymes related to NO2−-N conversion based on KEGG database. As shown in Fig. 6a, nitrite can be reduced to nitrogen (NO2−-N→N2) through denitrification and ammonia nitrogen (NO2−-N→NH4+-N) through dissimilatory nitrate reduction to ammonium (DNRA), in addition to being removed by anammox. The nitrite reductase (ammonia-forming) content of R2 was significantly higher than that of R1, while nitrite reductase (NO-forming) and nitric oxide reductase content of R2 was lower than that of R1. It had been reported that some DNRA bacteria can conduct DNRA process with sulfide (S2−) or elemental sulfur (S0) as electron donors45. And sulfide had an inhibitory effect on nitrous oxide reductase and nitric oxide reductase, which can inhibit the denitrification reaction, have an inhibitory effect on nitrite reductase (NO-forming) due to the accumulation of NO and promote the nitrite reduction reaction by the DNRA process24,25,46. In addition, heme was involved in the formation of nitrite reductase (ammonia-forming)47. Robertson et al. found that the addition of Fe2+ improved DNRA and inhibited denitrification48,49. It is postulated that the iron ions and sulfur ions released by FeS encouraged the occurrence of DNRA process and somehow decreased the denitrification reaction. Therefore, the removal rates of NO2−-N in the two reactors were significantly different, and the removal rates of NH4+-N were similar. This may also account for the relatively low abundance of denitrifying bacteria in R2. Moreover, Fig. 6b showed the predicted metabolism function of the two reactors’ communities, and the results indicated that the metabolic function of R2 was slightly higher than that of R1. It can be seen that the addition of FeS to the anammox reactor can increase microbial metabolism.
Fig. 6: Prediction of community functions based on KEGG.

a Nitrogen invertase content; b metabolism functions.

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Engineering significance
As a new type of environmentally-friendly biological nitrogen removal process, the anammox process has been a research hotspot, but it still encounters some issues to limit its wider application. Anammox bacteria are slow-growing microorganisms, and are sensitive to environmental conditions, such as salinity and organic carbon50. Another challenge of the anammox process system is the maintenance of effluent quality since about 10% nitrate would be produced in the anammox reaction, failing to meet discharge standards51.
In this study, the start-up time of the anammox reactor was shortened and the nitrogen removal rate was significantly increased with the addition of FeS. There were mainly two reasons: On one hand, FeS promoted the formation of anammox granular sludge and increased the abundance of anammox bacteria; on the other hand, FeS stimulated the synthesis of the heme c, which participated in the synthesis of a variety of enzymes. In addition, FeS can promote the DNRA process by inhibiting denitrification. Microbial oxidation of FeS, which links to the efficiency of denitrification, DNRA and anammox, plays an important role in the N cycle and S cycle15. According to previous report, FeS could function as an alternative electron donor for sulfur-dependent autotrophic denitrification52. Nitrate reduction was achieved by using pyrrhotite as the biofilter medium and autotrophic denitrifiers as seed in lab17. And DNRA process could occur due to HS− release18. This study found that FeS could promote the start-up of anammox process and promote the nitrite reduction reaction by the DNRA process through inhibiting denitrification. Therefore, it is possible to couple anammox with sulfur-autotrophic DNRA or sulfur-autotrophic denitrification in full-scale application by adding FeS to improve the total nitrogen removal efficiency. More

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