Quantifying taxonomy-function associations across hierarchical scales of bacterial nitrogen cycling

Mingli Jiang , Yanni Huang , Zhiming Wu , Qian Zhu , Qian Li , Kaihua Pan , Mingliang Zhang , Liang Shi , Jiguo Qiu , Pengfa Li , Xin Yan , Yiyong Zhu , Qing Hong

Soil Ecology Letters ›› 2026, Vol. 8 ›› Issue (5) : 260460

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Soil Ecology Letters ›› 2026, Vol. 8 ›› Issue (5) :260460 DOI: 10.1007/s42832-026-0460-1
RESEARCH ARTICLE
Quantifying taxonomy-function associations across hierarchical scales of bacterial nitrogen cycling
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Abstract

Microbes drive global nitrogen cycling, yet the extent to which taxonomic identity is associated with functional potential across bacterial diversity remains poorly quantified. Using 73472 representative bacterial genomes, we develop a quantitative framework integrating Information Gain analysis, functional classification, and molecular evolutionary analysis across six nitrogen cycling pathways and five taxonomic ranks. Association strength increases monotonically from phylum to genus level across all six pathways, with genus-level associations ranging from 39.5% (ANRA) to 67.5% (DNRA) among pathways with substantial prevalence (NIT excluded due to its extremely low global prevalence of 0.3%, which mathematically amplifies normalized IG values). Hierarchical clustering identifies four class-level functional archetypes—Functionally Inactive, Functionally Moderate, N-Retention Dominant, and Nitrification Specialist—among 77 bacterial classes, largely stable across genome source environments. At genus level, 1281 genera resolve into five ecological strategies spanning from single-direction specialists to genera maintaining both nitrogen retention and loss capacities. Molecular evolutionary analysis of 13 genes reveals that sequence conservation operates partially independently of pathway-level functional associations, generating four systematic decoupling patterns: congruent conservation for NF (nifH), under-conservation for DNRA (nrfA), over-conservation for DNN (napA), and gene-specific heterogeneity within DNF (nirS versus nirK). This framework establishes quantitative baselines that enable probabilistic inference of nitrogen cycling capabilities from taxonomic composition, with applications in amplicon-based community analysis, targeted cultivation, and biogeochemical modeling.

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Keywords

nitrogen cycling / taxonomy-function associations / functional archetypes / comparative genomics / sequence conservation

Highlight

● Establishes a quantitative framework for predicting nitrogen cycling potential from bacterial taxonomic identity.

● Reveals that taxonomy-function association strength is pathway-specific, enabling targeted functional inference with explicit reliability estimates.

● Identifies class-level functional archetypes and genus-level ecological strategies as intrinsic genomic properties stable across sampling environments.

● Reveals that pathway-level taxonomy-function associations and gene-level sequence conservation operate as partially independent dimensions, manifesting as four systematic decoupling patterns.

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Mingli Jiang, Yanni Huang, Zhiming Wu, Qian Zhu, Qian Li, Kaihua Pan, Mingliang Zhang, Liang Shi, Jiguo Qiu, Pengfa Li, Xin Yan, Yiyong Zhu, Qing Hong. Quantifying taxonomy-function associations across hierarchical scales of bacterial nitrogen cycling. Soil Ecology Letters, 2026, 8(5): 260460 DOI:10.1007/s42832-026-0460-1

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References

[1]

Anantharaman, K., Brown, C.T., Hug, L.A., Sharon, I., Castelle, C.J., Probst, A.J., Thomas, B.C., Singh, A., Wilkins, M.J., Karaoz, U., Brodie, E.L., Williams, K.H., Hubbard, S.S., Banfield, J.F., 2016. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nature Communications7, 13219.

[2]

Andam, C.P., Gogarten, J.P., 2011. Biased gene transfer in microbial evolution. Nature Reviews Microbiology9, 543–555.

[3]

Arnold, B.J., Huang, I.T., Hanage, W.P., 2022. Horizontal gene transfer and adaptive evolution in bacteria. Nature Reviews Microbiology20, 206–218.

[4]

Aziz, R.K., Bartels, D., Best, A.A., DeJongh, M., Disz, T., Edwards, R.A., Formsma, K., Gerdes, S., Glass, E.M., Kubal, M., Meyer, F., Olsen, G.J., Olson, R., Osterman, A.L., Overbeek, R.A., McNeil, L.K., Paarmann, D., Paczian, T., Parrello, B., Pusch, G.D., Reich, C., Stevens, R., Vassieva, O., Vonstein, V., Wilke, A., Zagnitko, O., 2008. The RAST server: rapid annotations using subsystems technology. BMC Genomics9, 75.

[5]

Barberán, A., Ramirez, K.S., Leff, J.W., Bradford, M.A., Wall, D.H., Fierer, N., 2014. Why are some microbes more ubiquitous than others? Predicting the habitat breadth of soil bacteria. Ecology Letters17, 794–802.

[6]

Benjamini, Y., Hochberg, Y., 1995. Controlling the false discovery rate - a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B: Statistical Methodology57, 289–300.

[7]

Buchfink, B., Xie, C., Huson, D.H., 2015. Fast and sensitive protein alignment using DIAMOND. Nature Methods12, 59–60.

[8]

Burch, C.L., Romanchuk, A., Kelly, M., Wu, Y.F., Jones, C.D., 2023. Empirical evidence that complexity limits horizontal gene transfer. Genome Biology and Evolution15, evad089.

[9]

Canty, A., Ripley, B.D., 2017. Boot: Bootstrap R (S-Plus) Functions. R Package Version 1.3–20. CRAN R Project.

[10]

Daims, H., Lücker, S., Wagner, M., 2016. A new perspective on microbes formerly known as nitrite-oxidizing bacteria. Trends in Microbiology24, 699–712.

[11]

Dean, A.M., Thornton, J.W., 2007. Mechanistic approaches to the study of evolution: the functional synthesis. Nature Reviews Genetics8, 675–688.

[12]

Dos Santos, P.C., Fang, Z., Mason, S.W., Setubal, J.C., Dixon, R., 2012. Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC Genomics13, 162.

[13]

Durand, S., Guillier, M., 2021. Transcriptional and post-transcriptional control of the nitrate respiration in bacteria. Frontiers in Molecular Biosciences8, 667758.

[14]

Goberna, M., Verdú, M., 2016. Predicting microbial traits with phylogenies. The ISME Journal10, 959–967.

[15]

Gout, J.F., Kahn, D., Duret, L., Consortium, P.P.G., 2010. The relationship among gene expression, the evolution of gene dosage, and the rate of protein evolution. PLoS Genetics6, e1000944.

[16]

Gowda, K., Ping, D., Mani, M., Kuehn, S., 2022. Genomic structure predicts metabolite dynamics in microbial communities. Cell185, 530–546.e25.

[17]

Hug, L.A., Baker, B.J., Anantharaman, K., Brown, C.T., Probst, A.J., Castelle, C.J., Butterfield, C.N., Hernsdorf, A.W., Amano, Y., Ise, K., Suzuki, Y., Dudek, N., Relman, D.A., Finstad, K.M., Amundson, R., Thomas, B.C., Banfield, J.F., 2016. A new view of the tree of life. Nature Microbiology1, 16048.

[18]

Isobe, K., Allison, S.D., Khalili, B., Martiny, A.C., Martiny, J.B.H., 2019. Phylogenetic conservation of bacterial responses to soil nitrogen addition across continents. Nature Communications10, 2499.

[19]

Jaccard, P., 1901. Étude de la distribution florale dans une portion des Alpes et du Jura. Bulletin de la Societe Vaudoise des Sciences Naturelles37, 547–579.

[20]

Jenks, G.F., Caspall, F.C., 1971. Error on choroplethic maps: definition, measurement, reduction. Annals of the Association of American Geographers61, 217–244.

[21]

Kanehisa, M., Furumichi, M., Sato, Y., Kawashima, M., Ishiguro-Watanabe, M., 2023. KEGG for taxonomy-based analysis of pathways and genomes. Nucleic Acids Research51, D587–D592.

[22]

Katoh, K., Standley, D.M., 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution30, 772–780.

[23]

Klotz, M.G., Stein, L.Y., 2008. Nitrifier genomics and evolution of the nitrogen cycle. FEMS Microbiology Letters278, 146–156.

[24]

Kosakovsky Pond, S.L., Frost, S.D.W., 2005. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Molecular Biology and Evolution22, 1208–1222.

[25]

Kuusemets, L., Mander, Ü., Escuer-Gatius, J., Astover, A., Kauer, K., Soosaar, K., Espenberg, M., 2025. Interactions of fertilisation and crop productivity in soil nitrogen cycle microbiome and gas emissions. Soil11, 1–15.

[26]

Kuypers, M.M.M., Marchant, H.K., Kartal, B., 2018. The microbial nitrogen-cycling network. Nature Reviews Microbiology16, 263–276.

[27]

Landis, J.R., Koch, G.G., 1977. The measurement of observer agreement for categorical data. Biometrics33, 159–174.

[28]

Langille, M.G.I., Zaneveld, J., Caporaso, J.G., McDonald, D., Knights, D., Reyes, J.A., Clemente, J.C., Burkepile, D.E., Vega Thurber, R.L., Knight, R., Beiko, R.G., Huttenhower, C., 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature Biotechnology31, 814–821.

[29]

Lin, Y.X., Hu, H.W., Gao, G.F., Cai, Y.J., 2023. Editorial: nitrogen-cycling microorganisms under global change: response and feedback. Frontiers in Microbiology14, 1166306.

[30]

Litchman, E., Klausmeier, C.A., Schofield, O.M., Falkowski, P.G., 2007. The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecology Letters10, 1170–1181.

[31]

Liu, S.Y., Dai, J.C., Wei, H.H., Li, S.Y., Wang, P., Zhu, T.B., Zhou, J.Z., Qiu, D.R., 2021. Dissimilatory nitrate reduction to ammonium (DNRA) and denitrification pathways are leveraged by cyclic AMP receptor protein (CRP) paralogues based on electron donor/acceptor limitation in Shewanella loihica PV-4. Applied and Environmental Microbiology87, e01964–20.

[32]

Louca, S., Parfrey, L.W., Doebeli, M., 2016. Decoupling function and taxonomy in the global ocean microbiome. Science353, 1272–1277.

[33]

Louca, S., Polz, M.F., Mazel, F., Albright, M.B.N., Huber, J.A., O’Connor, M.I., Ackermann, M., Hahn, A.S., Srivastava, D.S., Crowe, S.A., Doebeli, M., Parfrey, L.W., 2018. Function and functional redundancy in microbial systems. Nature Ecology & Evolution2, 936–943.

[34]

Lynch, M., 2007. The Origins of Genome Architecture. Sunderland: Sinauer.

[35]

Maechler, M., Rousseeuw, P., Struyf, A., Hubert, M., Hornik, K., 2018. Cluster: Cluster Analysis Basics and Extentions. R Package Version 2.0.7-1.

[36]

Martiny, A.C., Treseder, K., Pusch, G., 2013. Phylogenetic conservatism of functional traits in microorganisms. The ISME Journal7, 830–838.

[37]

McCutcheon, J.P., Moran, N.A., 2012. Extreme genome reduction in symbiotic bacteria. Nature Reviews Microbiology10, 13–26.

[38]

McNeish, D., Stapleton, L.M., 2016. Modeling clustered data with very few clusters. Multivariate Behavioral Research51, 495–518.

[39]

Milligan, G.W., Cooper, M.C., 1988. A study of standardization of variables in cluster analysis. Journal of Classification5, 181–204.

[40]

Ming, Y.Z., Al, M.A., Zhang, D.D., Zhu, W.G., Liu, H.P., Cai, L.L., Yu, X.L., Wu, K., Niu, M.Y., Zeng, Q.L., He, Z.L., Yan, Q.Y., 2024. Insights into the evolutionary and ecological adaption strategies of nirS- and nirK-type denitrifying communities. Molecular Ecology33, e17507.

[41]

Morris, J.J., Lenski, R.E., Zinser, E.R., 2012. The black queen hypothesis: evolution of dependencies through adaptive gene loss. mBio3, e00036–12.

[42]

Mosley, O.E., Gios, E., Close, M., Weaver, L., Daughney, C., Handley, K.M., 2022. Nitrogen cycling and microbial cooperation in the terrestrial subsurface. The ISME Journal16, 2561–2573.

[43]

Mukherjee, S., Stamatis, D., Bertsch, J., Ovchinnikova, G., Sundaramurthi, J.C., Lee, J., Kandimalla, M., Chen, I.M.A., Kyrpides, N.C., Reddy, T.B.K. 2021. Genomes OnLine Database (GOLD) v.8: overview and updates. Nucleic Acids Research49, D723–D733.

[44]

Nei, M., Li, W.H., 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceedings of the National Academy of Sciences of the United States of America76, 5269–5273.

[45]

Nelson, M.B., Martiny, A.C., Martiny, J.B.H., 2016. Global biogeography of microbial nitrogen-cycling traits in soil. Proceedings of the National Academy of Sciences of the United States of America113, 8033–8040.

[46]

Ochman, H., Lawrence, J.G., Groisman, E.A., 2000. Lateral gene transfer and the nature of bacterial innovation. Nature405, 299–304.

[47]

Parks, D.H., Chuvochina, M., Chaumeil, P.A., Rinke, C., Mussig, A.J., Hugenholtz, P., 2020. A complete domain-to-species taxonomy for Bacteria and Archaea. Nature Biotechnology38, 1079–1086.

[48]

Parks, D.H., Chuvochina, M., Rinke, C., Mussig, A.J., Chaumeil, P.A., Hugenholtz, P., 2022. GTDB: an ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy. Nucleic Acids Research50, D785–D794.

[49]

Parks, D.H., Rinke, C., Chuvochina, M., Chaumeil, P.A., Woodcroft, B.J., Evans, P.N., Hugenholtz, P., Tyson, G.W., 2017. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nature Microbiology2, 1533–1542.

[50]

Philippot, L., Andersson, S.G.E., Battin, T.J., Prosser, J.I., Schimel, J.P., Whitman, W.B., Hallin, S., 2010. The ecological coherence of high bacterial taxonomic ranks. Nature Reviews Microbiology8, 523–529.

[51]

Potter, L., Angove, H., Richardson, D., Cole, J., 2001. Nitrate reduction in the periplasm of gram-negative bacteria. Advances in Microbial Physiology45, 51–112.

[52]

Prosser, J.I., Hink, L., Gubry-Rangin, C., Nicol, G.W., 2020. Nitrous oxide production by ammonia oxidizers: physiological diversity, niche differentiation and potential mitigation strategies. Global Change Biology26, 103–118.

[53]

R Foundation, 2016. The R Project for Statistical Computing [Online]. Vienna: R Foundation for Statistical Computing. Available at the website of R-project.org/.

[54]

Raymond, J., Siefert, J.L., Staples, C.R., Blankenship, R.E., 2004. The natural history of nitrogen fixation. Molecular Biology and Evolution21, 541–554.

[55]

Richardson, D.J., 2000. Bacterial respiration: a flexible process for a changing environment. Microbiology146, 551–571.

[56]

Rousseeuw, P.J., 1987. Silhouettes: a graphical aid to the interpretation and validation of cluster analysis. Journal of Computational and Applied Mathematics20, 53–65.

[57]

Royalty, T.M., Steen, A.D., Tringe, S.G., 2019. Quantitatively partitioning microbial genomic traits among taxonomic ranks across the microbial tree of life. mSphere4, 10–1128.

[58]

Shannon, C.E., 1948. A mathematical theory of communication. Bell System Technical Journal27, 379–423.

[59]

Shoval, O., Sheftel, H., Shinar, G., Hart, Y., Ramote, O., Mayo, A., Dekel, E., Kavanagh, K., Alon, U., 2012. Evolutionary trade-offs, Pareto optimality, and the geometry of phenotype space. Science336, 1157–1160.

[60]

Simonsen, A.K., 2022. Environmental stress leads to genome streamlining in a widely distributed species of soil bacteria. The ISME Journal16, 423–434.

[61]

Sparacino-Watkins, C., Stolz, J.F., Basu, P., 2014. Nitrate and periplasmic nitrate reductases. Chemical Society Reviews43, 676–706.

[62]

Stamatakis, A., 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics30, 1312–1313.

[63]

Tu, Q.C., Lin, L., Cheng, L., Deng, Y., He, Z.L., 2019. NCycDB: a curated integrative database for fast and accurate metagenomic profiling of nitrogen cycling genes. Bioinformatics35, 1040–1048.

[64]

Wang, P.D., Li, J.L., Luo, X.Q., Ahmad, M., Duan, L., Yin, L.Z., Fang, B.Z., Li, S.H., Yang, Y.C., Jiang, L., Li, W.J., 2022. Biogeographical distributions of nitrogen-cycling functional genes in a subtropical estuary. Functional Ecology36, 187–201.

[65]

Wilcoxon, F., 1992. Individual comparisons by ranking methods. In: Kotz, S., Johnson, N.L., eds. Breakthroughs in Statistics: Methodology and Distribution. New York: Springer, 196–202.

[66]

Xu, L., Zakem, E., Weissman, J.L., 2025. Improved maximum growth rate prediction from microbial genomes by integrating phylogenetic information. Nature Communications16, 4256.

[67]

Yan, X.Y., Shan, J., Wang, X.M., Wang, B.Z., Liu, S.J., Zhang, P., Zhang, Y., Ling, J.R., Deng, O.P., Wang, C., Gu, B.J., Yan, X.Y., Shan, J., Wang, X.M., Wang, B.Z., Liu, S.J., Zhang, P., Zhang, Y., Ling, J.R., Deng, O.P., Wang, C., Gu, B.J., 2025. Uncovering the soil nitrogen cycle from microbial pathways to global sustainability. Nitrogen Cycling1, e002.

[68]

Yu, Z.S., Gao, Q., Guo, X., Peng, J.L., Qi, Q., Chen, X.W., Gao, M.Y., Mo, C.H., Feng, Z.Z., Wong, M.H., Yang, Y.F., Li, H., 2023. Phylogenetic conservation of soil microbial responses to elevated tropospheric ozone and nitrogen fertilization. mSystems8, e00721–22.

[69]

Zumft, W.G., 1997. Cell biology and molecular basis of denitrification. Microbiology and Molecular Biology Reviews61, 533–616.

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