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Frontiers of Environmental Science & Engineering

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Front. Environ. Sci. Eng.    2018, Vol. 12 Issue (3) : 10    https://doi.org/10.1007/s11783-018-1035-x
REVIEW ARTICLE
Anaerobic ammonia oxidizing bacteria: ecological distribution, metabolism, and microbial interactions
Dawen Gao(), Xiaolong Wang, Hong Liang, Qihang Wei, Yuan Dou, Longwei Li
State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology, Harbin 150090, China
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Abstract

The unique characteristics of anammox bacteria were reviewed.

Ecological distribution and nitrogen loss contributions were well documented.

Ecological interactions between anammox bacteria and other organisms were discussed.

Anammox (ANaerobic AMMonia OXidation) is a newly discovered pathway in the nitrogen cycle. This discovery has increased our knowledge of the global nitrogen cycle and triggered intense interest for anammox-based applications. Anammox bacteria are almost ubiquitous in the suboxic zones of almost all types of natural ecosystems and contribute significant to the global total nitrogen loss. In this paper, their ecological distributions and contributions to the nitrogen loss in marine, wetland, terrestrial ecosystems, and even extreme environments were reviewed. The unique metabolic mechanism of anammox bacteria was well described, including the particular cellular structures and genome compositions, which indicate the special evolutionary status of anammox bacteria. Finally, the ecological interactions among anammox bacteria and other organisms were discussed based on substrate availability and spatial organizations. This review attempts to summarize the fundamental understanding of anammox, provide an up-to-date summary of the knowledge of the overall anammox status, and propose future prospects for anammox. Based on novel findings, the metagenome has become a powerful tool for the genomic analysis of communities containing anammox bacteria; the metabolic diversity and biogeochemistry in the global nitrogen budget require more comprehensive studies.
Keywords Anammox      Metabolism      Metagenome      Ecological distribution      Microbial interactions     
Corresponding Author(s): Dawen Gao   
Issue Date: 29 March 2018
 Cite this article:   
Dawen Gao,Xiaolong Wang,Hong Liang, et al. Anaerobic ammonia oxidizing bacteria: ecological distribution, metabolism, and microbial interactions[J]. Front. Environ. Sci. Eng., 2018, 12(3): 10.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-018-1035-x
https://academic.hep.com.cn/fese/EN/Y2018/V12/I3/10
Fig.1  Numbers of anammox-related SCI publication from 1995 to 2017 (data from the search result on WEB OF SCIENCETM, THOMSON REUTERSTM)
Genus Species Reference
Candidatus Anammoxoglobus Candidatus Anammoxoglobus propionicus NCBI website
Candidatus Anammoxoglobus sulfate Liu et al. [5]
Candidatus Brocadia Candidatus Brocadia anammoxidans NCBI website
Candidatus Brocadia fulgida NCBI website
Candidatus Brocadia sinica NCBI website
Candidatus Brocadia brasiliensis NCBI website
Candidatus Brocadia caroliniensis NCBI website
Candidatus Jettenia Candidatus Jettenia asiatica NCBI website
Candidatus Jettenia moscovienalis NCBI website
Candidatus Jettenia caeni NCBI website
Candidatus Kuenenia Candidatus Kuenenia stuttgartiensis NCBI website
Candidatus Scalindua Candidatus Scalindua brodae NCBI website
Candidatus Scalindua wagneri NCBI website
Candidatus Scalindua rubra NCBI website
Candidatus Scalindua marina NCBI website
Candidatus Scalindua sorokinii Kuypers et al. [6]
Candidatus Scalindua arabica Woebken et al. [7]
Candidatus Scalindua sinooifield Li et al. [8]
Candidatus Scalindua zhenghei Hong et al. [9]
Candidatus Scalindua Profunda van de Vossenberg et al. [10]
Candidatus Scalindua richardsii Fuchsman et al. [11]
Candidatus Anammoximicrobium Candidatus Anammoximicrobium moscowii NCBI website
Tab.1  Candidatus Genera and species of anammox bacteria described so far
Ecosystem Location Activity and Contribution Abundance Species Depth Reference
Ocean water column Black Sea 3–4 fmol/(cell·d);>40% contribution 1900 cells/mL; 75% of all cells Scalindua sorokinii 90–100 m depth Kuyper et al. [6]
South Atlantic, Benguela 4.5 fmol/(cell·d) 2.2 × 104 cells/mL; 1% of all cells Scalindua sorokinii
Scalindua brodae		 40–130 m depth Woebken et al. [7]
Kuypers et al. [17]
Pacific of Iquique, Chile 0.24–0.7 nmol/(L·h) 3000 cells/mL; 0.45% of all cells Scalindua sorokinii 50 depth Thamdrup et al. [55]
Arabian Sea OMZ 0.03–0.1 nmol/(L·h); 8%–21% 1.7–4.1 × 105copies 16S rRNA/mL Scalindua arabica 150 m depth
650 m depth		 Bulow et al. [56]
Pitcher et al. [57]
Coast of Peru 0.4–2.4 fmol/(cell·d) 0.2–10 × 107cells/L;
0–3.1% of all cells		 Scalindua sorokinii
Scalindua brodae		 0–600 m depth Hamersley et al. [58]
Ocean sediments Arctic coasts, Greenland 0.23 fmol/(cell·d); 1%–35% 0.23 × 108 cells/mL; 25% of all cells ND 36–100 m depth Rysgaard et al. [59]
Schmid et al. [19]
South China Sea ND 1.2–7.2 × 104 hzo copies/g(dry) Scalindua 1657 m depth Hong et al. [9]
Equatorial Western Pacific ND 4.0 × 103–1.2 × 104 hzo copies/g(dry) Scalindua Surface sediment cores Hong et al. [54]
Golfo Dulce, Costa Rica 0.08–0.23 fmol/(cell·d) 0.021–1.1 × 108 cells/mL Scalindua 55 m water depth Schmid et al. [19]
Arctic fjord, Barents Sea Spitsbergen 0.24 fmol/(cell·d); 5%–23% 0.78 × 108 cells/mL; 8.6% of all cells Scalindua 50–211 m depth Gihring et al. [60]
Schmid et al. [19]
North Sea, Terschelling 0–3000 nmol/(L·h); 0%–29% contribution 3 × 103–1.5 × 10716S rRNA copies /g Scalindua 9–49 m depth Bale et al. [61]
Gullmar Fjord, Sweden 0.6–4.8 fmol/(cell·d); 23%–47% 1.6–4.7 × 108 cells/g Scalindua 117 m depth Brandsma et al. [62]
Wetland ecosystem Pearl River Estuary 1–2.6 μmol/(L·h); 3.8%–7.0% 1.4–20 × 108 hzo copies/g(dry) Brocadia, Kuenenia 0–5 cm Wang et al. [27]
Cape Fear River
Estuary, USA		 3.8%–16.5% <1.3–84 × 105 16S rRNA copies/g Except Anammoxoglobus 1 m water depth
Top 3 cm		 Dale et al. [35]
Yangtze Estuary 0.94–6.61?nmol/(g·h); 7%–13% 2.63–15.6 × 106 16S rRNA copies/g Brocadia, Kuenenia Scalindua Surface soil Hou et al. [29]
Paddy soil, Jiaxing, China 0.5–2.9?nmol/(g·h); 4%–37% 4.4 × 106 cells/g Jettenia, Kuenenia, Anammoxoglobus 100 cm depth Zhu et al. [39]
Southern China, Paddy Soil 0.27–5.25 nmol/(g·h); 0.6%–15% 1.2–9.7 × 104 hzs copies/g dry soil Brocadia,
Kuenenia		 0–20 cm Yang et al. [63]
Hunan, China, Paddy 0.33–0.64 nmol/(g·h); 31%–41% 0.7–1.4 × 107 hzs copies/g dry soil Brocadia
Kuenenia		 0–20 cm Li et al. [64]
Jiangsu, China
Paddy ditches		 4.4–23.8 nmol/(g·d); 2.1%–18.8% 1.9–12 × 104 hzs copies/g dry sediment Kuenenia, Brocadia, Anammoxoglobus 0–10 cm Shen et al. [65]
Hongkong Dongjiang River ND 0.3–11 × 106 16S rRNA copies/g(dry) Brocadia, Jettenia Surface: 0–5 cm Boog et al. [66]
Canada, Ground water, 13–31 nmol/(L·h); 18%–36% 5.2%–20.8% of 16S rRNA Except Anammoxoglobus 1.9–7.5 m Moore et al. [42]
Soil North Carolina 0.78 nmol/(g·d); 11% 5–16 × 105 hzo copies/g dry soil Jettenia 30 cm depth Long et al. [48]
Tab.2  Distributions, contributions, and activities of anammox bacteria in different natural environments (ND: no data)
Origin Predicted genes rRNA Nitrite reductase
(NIR)		 Nitrate reductase:
(NAR/NXR)		 Hydrazine synthesis
(HZS)		 Hydrazine/ Hydroxylamine oxidoreductase
(HZO/HAO)		 Ammonia transport Nitrite
transport		 Nitrate
transport		 Reference
Scalindua profunda from JGI
(2017108002, 2022004002) 		4756 genes:
3347 genes matched in database;
98 genes with particular metabolism		 3 Cyt cd1nirS:
similar to HAO protein		 nxrA/narG:
scal00861–00868
(highly expressed)		 hzsA: scal01318;
hzsBC gene: scal00025		 9 genes: except kuste2457;
HZO function: scal03295;
Possible HZO function: scal01317,02116		 12 amtB genes:
scal00587–00596
2 partial genes:
scal0168,03708		 4 genes: scal0947, 00975,00416;
focA from FNT family similar to E.colinirC		 1 narK type I gene: scal03007 van de Vossenberg et al. [10]
Kuenenia stuttgartiensis from EMBL
(CT030148,573071–573074) 		4664 genes:
3279 (70.3%) genes matched in database;
200 genes relevant to particular metabolism		 1 Cyt cd1nirS:
kuste4136–4140		 nar gene:
kustd1699–1713;
nxrG: kustd1700;
nxrH: kustd1703;
nxrI is absent heme
b-containing:
kustd1704 or kustd1709		 hzsCBA:
kuste2859–2861		 10 genes:
kustc0458,0694,1061,
kuste2435,2457,2479,4574, kusta0043; kustd1340,2021;
HAO function: kustc1061
HZO function: kusta0043, kustc1061,0694		 5 amtB genes 1 gene: kusta3055, similar to E.coli nirC;
5 focA genes: kusta0004,0009,1720,1721,4324		 3 genes: kuste2335,2308 and kustd2047;
first two are similar to scal03007		 Strous et al. [78]
Brocadia fulgida 2726 contigs:
536 ORFs		 ND Missing:
only 2 possible genes		 4 narG genes;
1 narH gene: similar to kustd1703		 hzsCBA is highly mapped 9 genes: except kuste2457; HZO function: kustc0694, kustd1340 3 amtB genes 1 focA gene 1 nark gene Gori et al. [80]
Jettenia asiatica 37432 contigs ND Cu-containing nirK:
contig1180 and 21694		 nxrG and nxrH matched 2 contigs:
covered hzsCBA subunit genes		 8 genes: except kuste2479, kustd2021;
HAO function: kustc1061;
HZO function: kustd1340, kustc0694		 7 contigs:
similar to 5 genes of Kuenenia		 3 genes:
similar to focA genes of Kuenenia		 2 contigs:
similar to 2 narK genes of Kuenenia		 Hu et al. [81]
Tab.3  Genome information of four anammox bacteria species (ND: no data)
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