PDF
Abstract
Anaerobic ammonium oxidation (anammox) plays a critical role in nitrogen loss in estuarine and marine environments. However, the mechanisms underlying the formation and maintenance of the anammox bacterial community remain unclear. This study analyzed the anammox bacterial diversity, community structure, and interspecific relationships in three estuaries along the Chinese coastline —the Changjiang Estuary (CJE), the Oujiang Estuary (OJE), and the Jiulong River Estuary (JLE) — as well as the South China Sea (SCS) to elucidate their community assembly mechanisms. The results indicated that the anammox bacterial community exhibited the highest ammonium concentration as well as the Shannon’s diversity index reflecting both species richness and evenness in the JLE. The lowest Shannon index was observed in the SCS. However, the anammox bacterial species richness was greatest in the CJE. Candidatus Scalindua was the predominant anammox bacteria identified in the coastal sediments, especially in the SCS sediments. Candidatus Brocadia and Candidatus Kuenenia were more abundant in the estuarine sediments, particularly in JLE, than in the SCS. Phylogenetic analysis revealed distinct differentiation among Candidatus Scalindua, Candidatus Brocadia, and Candidatus Kuenenia, with the former exhibiting a greater level of diversity. There was significant spatial heterogeneity in the anammox bacteria across the four regions, characterized by distinct distribution patterns for rare species. Low-abundance (rare) bacteria thrived in their native habitats, whereas abundant taxa displayed greater dispersal capabilities. An analysis of the community assembly mechanism suggested that ecological drift predominantly shaped the overall anammox bacterial community in the coastal sediments. Rare species were more susceptible to dispersal limitations and environmental selection. Co-occurrence network analysis identified Candidatus Scalindua as a keystone genus and highlighted that rare species may play a crucial role in maintaining the ecological stability of the anammox bacterial community in coastal sediments.
Special Topic: Ecology & Environmental Biology.
The online version contains supplementary material available at https://doi.org/10.1007/s42995-025-00315-8.
Keywords
Anammox bacteria
/
Community structure
/
Community assembly
/
Co-occurrence network
/
Rare species
Cite this article
Download citation ▾
Yu Zhang, Mingming Chen, Rui Du, Ehui Tan, Shuh-Ji Kao, Yao Zhang.
Critical roles of rare species in the anaerobic ammonium oxidizing bacterial community in coastal sediments.
Marine Life Science & Technology, 2025, 7(3): 507-522 DOI:10.1007/s42995-025-00315-8
| [1] |
AanderudZT, JonesSE, FiererN, LennonJT. Resuscitation of the rare biosphere contributes to pulses of ecosystem activity. Front Microbiol, 2015, 624.
|
| [2] |
Abdullah AlM, XueY, XiaoP, XuJ, ChenH, MoY, ShimetaJ, YangJ. Community assembly of microbial habitat generalists and specialists in urban aquatic ecosystems explained more by habitat type than pollution gradient. Water Res, 2022, 220. 118693
|
| [3] |
AiD, ChuC, EllwoodMDF, HouR, WangG. Migration and niche partitioning simultaneously increase species richness and rarity. Ecol Model, 2013, 258: 33-39.
|
| [4] |
AllanE, WeisserW, WeigeltA, RoscherC, FischerM, HillebrandH. More diverse plant communities have higher functioning over time due to turnover in complementary dominant species. Proc Natl Acad Sci USA, 2011, 108: 17034-17039.
|
| [5] |
BanerjeeS, SchlaeppiK, van der HeijdenMGA. Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol, 2018, 16: 567-576.
|
| [6] |
BrinLD, GiblinAE, RichJJ. Environmental controls of anammox and denitrification in southern New England estuarine and shelf sediments. Limnol Oceanogr, 2014, 59: 851-860.
|
| [7] |
CaiW-J, HuX, HuangW-J, MurrellMC, LehrterJC, LohrenzSE, ChouW-C, ZhaiW, HollibaughJT, WangY, ZhaoP, GuoX, GundersenK, DaiM, GongG-C. Acidification of subsurface coastal waters enhanced by eutrophication. Nat Geosci, 2011, 4: 766-770.
|
| [8] |
CampbellBJ, YuL, HeidelbergJF, KirchmanDL. Activity of abundant and rare bacteria in a coastal ocean. Proc Natl Acad Sci USA, 2011, 108: 12776-12781.
|
| [9] |
ChaseJM. Stochastic community assembly causes higher biodiversity in more productive environments. Science, 2010, 328: 1388-1391.
|
| [10] |
ChaseJM, MyersJA. Disentangling the importance of ecological niches from stochastic processes across scales. Philos Trans R Soc Lond B Biol Sci, 2011, 366: 2351-2363.
|
| [11] |
ChenC, TianL, ShengY, WangR, LiJ, ZhangD, ZhangC. Abundance, diversity, and community composition of anammox bacteria in sediments of Xiangshan Bay. China Reg Stud Mar Sci, 2021, 44101739
|
| [12] |
CroweSA, CanfieldDE, MucciA, SundbyB, MarangerR. Anammox, denitrification and fixed-nitrogen removal in sediments from the Lower St. Lawrence Estuary Biogeosci, 2012, 9: 4309-4321.
|
| [13] |
DaiT, ZhangY, TangY, BaiY, TaoY, HuangB, WenD. Identifying the key taxonomic categories that characterize microbial community diversity using full-scale classification: a case study of microbial communities in the sediments of Hangzhou Bay. Fems Microbiol Ecol, 2017, 93fiw150.
|
| [14] |
DaleOR, TobiasCR, SongB. Biogeographical distribution of diverse anaerobic ammonium oxidizing (anammox) bacteria in Cape Fear River Estuary. Environ Microbiol, 2009, 11: 1194-1207.
|
| [15] |
DamashekJ, FrancisCA. Microbial nitrogen cycling in estuaries: from genes to ecosystem processes. Estuar Coast, 2017, 41: 626-660.
|
| [16] |
DangH, ChenR, WangL, GuoL, ChenP, TangZ, TianF, LiS, KlotzMG. Environmental factors shape sediment anammox bacterial communities in hypernutrified Jiaozhou Bay, China. Appl Environ Microbiol, 2010, 76: 7036-7047.
|
| [17] |
DangH, ZhouH, ZhangZ, YuZ, HuaE, LiuX, JiaoN. Molecular detection of candidatus scalindua pacifica and environmental responses of sediment anammox bacterial community in the Bohai Sea. China Plos One, 2013, 8. e61330
|
| [18] |
DengY, JiangYH, YangY, HeZ, LuoF, ZhouJ. Molecular ecological network analyses. BMC Bioinform, 2012, 13113.
|
| [19] |
DevolAH. Denitrification, anammox, and N(2) production in marine sediments. Ann Rev Mar Sci, 2015, 7: 403-423.
|
| [20] |
DongLF, SmithCJ, PapaspyrouS, StottA, OsbornAM, NedwellDB. Changes in benthic denitrification, nitrate ammonification, and anammox process rates and nitrate and nitrite reductase gene abundances along an estuarine nutrient gradient (the Colne estuary, United Kingdom). Appl Environ Microbiol, 2009, 75: 3171-3179.
|
| [21] |
FetzerI, JohstK, SchaweR, BanitzT, HarmsH, ChatzinotasA. The extent of functional redundancy changes as species’ roles shift in different environments. Proc Natl Acad Sci USA, 2015, 112: 14888-14893.
|
| [22] |
FoziaZY, HouL, ZhangZ, ChenF, GaoD, YinG, HanP, DongH, LiangX, YangY, LiuM. Anaerobic ammonium oxidation (anammox) bacterial diversity, abundance, and activity in sediments of the Indus Estuary. Estuar Coast Shelf S, 2020, 243. 106925
|
| [23] |
FrancisCA, BemanJM, KuypersMM. New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J, 2007, 1: 19-27.
|
| [24] |
FuL, ChenY, LiS, HeH, MiT, ZhenY, YuZ. Shifts in the anammox bacterial community structure and abundance in sediments from the Changjiang Estuary and its adjacent area. Syst Appl Microbiol, 2019, 42: 383-396.
|
| [25] |
GalandPE, CasamayorEO, KirchmanDL, LovejoyC. Ecology of the rare microbial biosphere of the Arctic Ocean. Proc Natl Acad Sci USA, 2009, 106: 22427-22432.
|
| [26] |
GallowayJN, SchlesingerWH, LevyH, MichaelsA, SchnoorJL. Nitrogen fixation: Anthropogenic enhancement-environmental response. Global Biogeochem Cy, 1995, 9: 235-252.
|
| [27] |
GobetA, BoerSI, HuseSM, van BeusekomJE, QuinceC, SoginML, BoetiusA, RametteA. Diversity and dynamics of rare and of resident bacterial populations in coastal sands. ISME J, 2012, 6: 542-553.
|
| [28] |
HanP, HuangYT, LinJG, GuJD. A comparison of two 16S rRNA gene-based PCR primer sets in unraveling anammox bacteria from different environmental samples. Appl Microbiol Biotechnol, 2013, 97: 10521-10529.
|
| [29] |
HansonCA, FuhrmanJA, Horner-DevineMC, MartinyJB. Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol, 2012, 10: 497-506.
|
| [30] |
HirschMD, LongZT, SongB. Anammox bacterial diversity in various aquatic ecosystems based on the detection of hydrazine oxidase genes (hzoA/hzoB). Microb Ecol, 2011, 61: 264-276.
|
| [31] |
HouL, ZhengY, LiuM, GongJ, ZhangX, YinG, YouL. Anaerobic ammonium oxidation (anammox) bacterial diversity, abundance, and activity in marsh sediments of the Yangtze Estuary. J Geophys Res-Biogeo, 2013, 118: 1237-1246.
|
| [32] |
JaeschkeA, AbbasB, ZabelM, HopmansEC, SchoutenS, Sinninghe DamstéaJS. Molecular evidence for anaerobic ammonium-oxidizing (anammox) bacteria in continental shelf and slope sediments off northwest Africa. Limnol Oceanogr, 2009, 55: 365-376.
|
| [33] |
JiaX, Dini-AndreoteF, Falcao SallesJ. Community assembly processes of the microbial rare biosphere. Trends Microbiol, 2018, 26: 738-747.
|
| [34] |
JiaoL, WuJ, HeX, WenX, LiY, HongY. Significant microbial nitrogen loss from denitrification and anammox in the land-sea interface of low permeable sediments. Int Biodeter Biodegr, 2018, 135: 80-89.
|
| [35] |
JoussetA, BienholdC, ChatzinotasA, GallienL, GobetA, KurmV, KueselK, RilligMC, RivettDW, SallesJF, van der HeijdenMGA, YoussefNH, ZhangX, WeiZ, HolWHG. Where less may be more: how the rare biosphere pulls ecosystems strings. ISME J, 2017, 11: 853-862.
|
| [36] |
KaoSJ, LiuKK, HsuSC, ChangYP, DaiMH. North Pacific-wide spreading of isotopically heavy nitrogen during the last deglaciation: Evidence from the western Pacific. Biogeosciences, 2008, 5: 1641-1650.
|
| [37] |
KartalB, KuypersMM, LavikG, SchalkJ, Op den CampHJ, JettenMS, StrousM. Anammox bacteria disguised as denitrifiers: nitrate reduction to dinitrogen gas via nitrite and ammonium. Environ Microbiol, 2007, 9: 635-642.
|
| [38] |
KartalB, RattrayJ, van NiftrikLA, van de VossenbergJ, SchmidMC, WebbRI, SchoutenS, FuerstJA, DamsteJS, JettenMS, StrousM. Candidatus "Anammoxoglobus propionicus" a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol, 2007, 30: 39-49.
|
| [39] |
KartalB, van NiftrikL, RattrayJ, van de VossenbergJL, SchmidMC, Sinninghe DamsteJ, JettenMS, StrousM. Candidatus ‘Brocadia fulgida’: an autofluorescent anaerobic ammonium oxidizing bacterium. Fems Microbiol Ecol, 2008, 63: 46-55.
|
| [40] |
KoleffP, GastonKJ, LennonJJ. Measuring beta diversity for presence–absence data. J Anim Ecol, 2003, 72: 367-382.
|
| [41] |
LamP, KuypersMM. Microbial nitrogen cycling processes in oxygen minimum zones. Ann Rev Mar Sci, 2011, 3: 317-345.
|
| [42] |
LauroFM, McDougaldD, ThomasT, WilliamsTJ, EganS, RiceS, DeMaereMZ, TingL, ErtanH, JohnsonJ, FerrieraS, LapidusA, AndersonI, KyrpidesN, MunkAC, DetterC, HanCS, BrownMV, RobbFT, KjellebergS, et al.. The genomic basis of trophic strategy in marine bacteria. Proc Natl Acad Sci USA, 2009, 106: 15527-15533.
|
| [43] |
LiM, HongY, KlotzMG, GuJD. A comparison of primer sets for detecting 16S rRNA and hydrazine oxidoreductase genes of anaerobic ammonium-oxidizing bacteria in marine sediments. Appl Microbiol Biotechnol, 2010, 86: 781-790.
|
| [44] |
LiJ, QiP, LiR, WangJ, WangD. Carbon and nitrogen removal through Candidatus Brocadia sinica"-dominated simultaneous anammox and denitrification (SAD) process treating saline wastewater. Biochem Eng J, 2018, 140: 72-76.
|
| [45] |
LiY, GaoY, ZhangW, WangC, WangP, NiuL, WuH. Homogeneous selection dominates the microbial community assembly in the sediment of the Three Gorges Reservoir. Sci Total Environ, 2019, 690: 50-60.
|
| [46] |
LiX, QianW, HouL, LiuM, ChenZ, TongC. Human activity intensity controls the relative importance of denitrification and anaerobic ammonium oxidation across subtropical estuaries. CATENA, 2021, 202. 105260
|
| [47] |
LiangY, XiaoX, NuccioEE, YuanM, ZhangN, XueK, CohanFM, ZhouJ, SunB. Differentiation strategies of soil rare and abundant microbial taxa in response to changing climatic regimes. Environ Microbiol, 2020, 22: 1327-1340.
|
| [48] |
LindströmES, LangenhederS. Local and regional factors influencing bacterial community assembly. Environ Microbiol Rep, 2012, 4: 1-9.
|
| [49] |
MeyerRL, Risgaard-PetersenN, AllenDE. Correlation between anammox activity and microscale distribution of nitrite in a subtropical mangrove sediment. Appl Environ Microbiol, 2005, 71: 6142-6149.
|
| [50] |
MoY, ZhangW, YangJ, LinY, YuZ, LinS. Biogeographic patterns of abundant and rare bacterioplankton in three subtropical bays resulting from selective and neutral processes. ISME J, 2018, 12: 2198-2210.
|
| [51] |
MulderA, GraafAA, RobertsonLA, KuenenJG. Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. Fems Microbiol Ecol, 1995, 16: 177-184.
|
| [52] |
NaeherS, HuguetA, Roose-AmsalegCL, LavermanAM, FosseC, LehmannMF, DerenneS, ZopfiJ. Molecular and geochemical constraints on anaerobic ammonium oxidation (anammox) in a riparian zone of the Seine Estuary (France). Biogeochemistry, 2015, 123: 237-250.
|
| [53] |
NemergutDR, CostelloEK, HamadyM, LozuponeC, JiangL, SchmidtSK, FiererN, TownsendAR, ClevelandCC, StanishL, KnightR. Global patterns in the biogeography of bacterial taxa. Environ Microbiol, 2011, 13: 135-144.
|
| [54] |
NemergutDR, SchmidtSK, FukamiT, O’NeillSP, BilinskiTM, StanishLF, KnelmanJE, DarcyJL, LynchRC, WickeyP, FerrenbergS. Patterns and processes of microbial community assembly. Microbiol Mol Biol Rev, 2013, 77: 342-356.
|
| [55] |
PentonCR, DevolAH, TiedjeJM. Molecular evidence for the broad distribution of anaerobic ammonium-oxidizing bacteria in freshwater and marine sediments. Appl Environ Microbiol, 2006, 72: 6829-6832.
|
| [56] |
PhilippotL, SporA, HenaultC, BruD, BizouardF, JonesCM, SarrA, MaronPA. Loss in microbial diversity affects nitrogen cycling in soil. ISME J, 2013, 7: 1609-1619.
|
| [57] |
QianG, WangJ, KanJ, ZhangX, XiaZ, ZhangX, MiaoY, SunJ. Diversity and distribution of anammox bacteria in water column and sediments of the Eastern Indian Ocean. Int Biodeter Biodegr, 2018, 133: 52-62.
|
| [58] |
RabalaisNN, TurnerRE, DíazRJ, JustićD. Global change and eutrophication of coastal waters. Ices J Mar Sci, 2009, 66: 1528-1537.
|
| [59] |
RouskJ, BrookesPC, BaathE. Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl Environ Microbiol, 2009, 75: 1589-1596.
|
| [60] |
RussL, KartalB, Op den CampHJ, SollaiM, Le BruchecJ, CapraisJC, GodfroyA, Sinninghe DamsteJS, JettenMS. Presence and diversity of anammox bacteria in cold hydrocarbon-rich seeps and hydrothermal vent sediments of the Guaymas Basin. Front Microbiol, 2013, 4219.
|
| [61] |
SchmidM, TwachtmannU, KleinM, StrousM, JuretschkoS, JettenM, MetzgerJW, SchleiferKH, WagnerM. Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst Appl Microbiol, 2000, 23: 93-106.
|
| [62] |
SchmidM, WalshK, WebbR, RijpstraWI, van de Pas-SchoonenK, VerbruggenMJ, HillT, MoffettB, FuerstJ, SchoutenS, DamsteJS, HarrisJ, ShawP, JettenM, StrousM. Candidatus "Scalindua brodae", sp. nov., Candidatus "Scalindua wagneri", sp. nov., two new species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol, 2003, 26: 529-538.
|
| [63] |
ShaoS, LuanX, DangH, ZhouH, ZhaoY, LiuH, ZhangY, DaiL, YeY, KlotzMG. Deep-sea methane seep sediments in the Okhotsk Sea sustain diverse and abundant anammox bacteria. Fems Microbiol Ecol, 2014, 87: 503-516.
|
| [64] |
ShehzadA, LiuJ, YuM, QismatS, LiuJ, ZhangXH. Diversity, community composition and abundance of anammox bacteria in sediments of the North Marginal Seas of China. Microbes Environ, 2016, 31: 111-120.
|
| [65] |
StegenJC, LinX, KonopkaAE, FredricksonJK. Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J, 2012, 6: 1653-1664.
|
| [66] |
StegenJC, LinX, FredricksonJK, ChenX, KennedyDW, MurrayCJ, RockholdML, KonopkaA. Quantifying community assembly processes and identifying features that impose them. ISME J, 2013, 7: 2069-2079.
|
| [67] |
SteinLY, KlotzMG. The nitrogen cycle. Curr Biol, 2016, 26: R94-98.
|
| [68] |
StelzerRS, ScottJT. Predicting nitrate retention at the groundwater-surface water interface in Sandplain Streams. J Geophys Res-Biogeo, 2018, 123: 2824-2838.
|
| [69] |
StrousM, FuerstJA, KramerEH, LogemannS, MuyzerG, van de Pas-SchoonenKT, WebbR, KuenenJG, JettenMS. Missing lithotroph identified as new planctomycete. Nature, 1999, 400: 446-449.
|
| [70] |
StrousM, PelletierE, MangenotS, RatteiT, LehnerA, TaylorMW, HornM, DaimsH, Bartol-MavelD, WinckerP, BarbeV, FonknechtenN, VallenetD, SegurensB, Schenowitz-TruongC, MedigueC, CollingroA, SnelB, DutilhBE, Op den CampHJ, et al.. Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature, 2006, 440: 790-794.
|
| [71] |
TanE, ZouW, JiangX, WanX, HsuTC, ZhengZ, ChenL, XuM, DaiM, KaoSJ. Organic matter decomposition sustains sedimentary nitrogen loss in the Pearl River Estuary, China. Sci Total Environ, 2019, 648: 508-517.
|
| [72] |
TrimmerM, NichollsJC, DeflandreB. Anaerobic ammonium oxidation measured in sediments along the Thames estuary, United Kingdom. Appl Environ Microbiol, 2003, 69: 6447-6454.
|
| [73] |
van de GraafAA, MulderA, de BruijnP, JettenMS, RobertsonLA, KuenenJG. Anaerobic oxidation of ammonium is a biologically mediated process. Appl Environ Microbiol, 1995, 61: 1246-1251.
|
| [74] |
van de VossenbergJ, RattrayJE, GeertsW, KartalB, van NiftrikL, van DonselaarEG, Sinninghe DamsteJS, StrousM, JettenMS. Enrichment and characterization of marine anammox bacteria associated with global nitrogen gas production. Environ Microbiol, 2008, 10: 3120-3129.
|
| [75] |
van de VossenbergJ, WoebkenD, MaalckeWJ, WesselsHJ, DutilhBE, KartalB, Janssen-MegensEM, RoeselersG, YanJ, SpethD, GloerichJ, GeertsW, van der BiezenE, PlukW, FrancoijsKJ, RussL, LamP, MalfattiSA, TringeSG, HaaijerSC, et al.. The metagenome of the marine anammox bacterium ‘Candidatus Scalindua profunda’ illustrates the versatility of this globally important nitrogen cycle bacterium. Environ Microbiol, 2013, 15: 1275-1289.
|
| [76] |
van ElsasJD, ChiurazziM, MallonCA, ElhottovaD, KristufekV, SallesJF. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc Natl Acad Sci USA, 2012, 109: 1159-1164.
|
| [77] |
VipindasPV, KrishnanKP, RehithaTV, JabirT, DineshSL. Diversity of sediment associated Planctomycetes and its related phyla with special reference to anammox bacterial community in a high Arctic fjord. World J Microb Biot, 2020, 36107.
|
| [78] |
WangS, ZhuG, PengY, JettenMS, YinC. Anammox bacterial abundance, activity, and contribution in riparian sediments of the Pearl River estuary. Environ Sci Technol, 2012, 46: 8834-8842.
|
| [79] |
WellsNS, MaherDT, ErlerDV, HipseyM, RosentreterJA, EyreBD. Estuaries as sources and sinks of N2O across a land use gradient in Subtropical Australia. Global Biogeochem Cy, 2018, 32: 877-894.
|
| [80] |
WenX, HongY, WuJ, WangY. Optimization of a method for diversity analysis of anammox bacteria using high-throughput sequencing of 16S rRNA gene amplicon. J Microbiol Methods, 2020, 178. 106066
|
| [81] |
WoebkenD, LamP, KuypersMM, NaqviSW, KartalB, StrousM, JettenMS, FuchsBM, AmannR. A microdiversity study of anammox bacteria reveals a novel Candidatus Scalindua phylotype in marine oxygen minimum zones. Environ Microbiol, 2008, 10: 3106-3119.
|
| [82] |
WuJ, HongY, WenX, LiY, WangY, ChangX. Activity, abundance, and community composition of anaerobic ammonia–oxidizing (anammox) bacteria in sediment cores of the Pearl River Estuary. Estuar Coast, 2019, 43: 73-85.
|
| [83] |
WuJ, HongY, YeJ, LiY, LiuX, JiaoL, LiT, LiY, BinL, WangY. Diversity of anammox bacteria and contribution to the nitrogen loss in surface sediment. Int Biodeter Biodegr, 2019, 142: 227-234.
|
| [84] |
XueY, ChenH, YangJR, LiuM, HuangB, YangJ. Distinct patterns and processes of abundant and rare eukaryotic plankton communities following a reservoir cyanobacterial bloom. ISME J, 2018, 12: 2263-2277.
|
| [85] |
YoosephS, NealsonKH, RuschDB, McCrowJP, DupontCL, KimM, JohnsonJ, MontgomeryR, FerrieraS, BeesonK, WilliamsonSJ, TovchigrechkoA, AllenAE, ZeiglerLA, SuttonG, EisenstadtE, RogersYH, FriedmanR, FrazierM, VenterJC. Genomic and functional adaptation in surface ocean planktonic prokaryotes. Nature, 2010, 468: 60-66.
|
| [86] |
ZhangL, OkabeS. Ecological niche differentiation among anammox bacteria. Water Res, 2020, 171. 115468
|
| [87] |
ZhengY, JiangX, HouL, LiuM, LinX, GaoJ, LiX, YinG, YuC, WangR. Shifts in the community structure and activity of anaerobic ammonium oxidation bacteria along an estuarine salinity gradient. J Geophys Res-Biogeo, 2016, 121: 1632-1645.
|
| [88] |
ZhengX, XuK, NaoumJ, LianY, WuB, HeZ, YanQ. Deciphering microeukaryotic–bacterial co-occurrence networks in coastal aquaculture ponds. Mar Life Sci Technol, 2023, 5: 44-55.
|
| [89] |
ZhouJ, NingD. Stochastic community assembly: does it matter in microbial ecology?. Microbiol Mol Biol Rev, 2017.
|
RIGHTS & PERMISSIONS
The Author(s)