Linking rhizosphere bacterial life-history strategies with wheat growth under drought stress

Abstract

The metabolic complexity of microorganisms can be simplified by classifying them into r-strategists and K-strategists. However, their associations with plant growth during drought remain largely unclear. Herein, we used the ribosomal RNA gene operon (rrn) copy number to characterize bacterial life-history strategies, with increased rrn copy numbers suggesting a shift from K- to r-strategies. We generated a series of bacterial communities with increased rrn copy numbers in rhizosphere. Drought decreased rhizosphere bacterial rrn copy numbers, rather than in root, indicating a prevalence of K-strategies during drought stress in rhizosphere. The rrn copy numbers of rhizosphere communities were negatively related to wheat growth during drought, while no significant associations were observed in control treatment. Rhizosphere bacterial communities with higher rrn copy numbers exhibited less community dissimilarity and tended to be more stable. Moreover, the abundance of most predicted functions decreased with rrn copy numbers in drought-stressed rhizosphere. Co-occurrence network analysis indicated that increased rrn copy numbers in rhizosphere community improved the proportion of negative to positive cohesion, implying more stable networks. Our findings bring up innovative knowledge about the relationships between microbial life-history strategies, communities and plant growth, and highlights the importance of plant-microorganism interactions for plant growth during stress.

Graphical abstract

Keywords

life-history strategies / rrn copy numbers / co-occurrence network / plant growth / drought stress

Highlight

	● Distinct life history strategies of rhizosphere bacterial communities were established using the dilution-to-extinction approach.
	● The life history strategies of rhizosphere bacterial communities influenced wheat growth during drought stress.
	● Bacterial life history strategies exhibited a significant impact on community assembly in rhizosphere.
	● A shift in rhizosphere bacterial life history strategies towards copiotrophy resulted in stable networks.

References

[1] Barberán, A., Bates, S.T., Casamayor, E.O., Fierer, N., 2012. Using network analysis to explore co-occurrence patterns in soil microbial communities. The ISME Journal6, 343–351.

[2] Bartelme, R.P., Custer, J.M., Dupont, C.L., Espinoza, J.L., Torralba, M., Khalili, B., Carini, P., Tringe, S.G., 2020. Influence of substrate concentration on the culturability of heterotrophic soil microbes isolated by high-throughput dilution-to-extinction cultivation. MSphere5, e00024–20.

[3] Berendsen, R.L., Vismans, G., Yu, K., Song, Y., de Jonge, R., Burgman, W.P., Burmolle, M., Herschend, J., Bakker, P.A.H.M., Pieterse, C.M.J., 2018. Disease-induced assemblage of a plant-beneficial bacterial consortium. The ISME Journal12, 1496–1507.

[4] Burns, R.G., DeForest, J.L., Marxsen, J., Sinsabaugh, R.L., Stromberger, M.E., Wallenstein, M.D., Weintraub, M.N., Zoppini, A., 2013. Soil enzymes in a changing environment: current knowledge and future directions. Soil Biology and Biochemistry58, 216–234.

[5] Cairns, J., Moerman, F., Fronhofer, E.A., Altermatt, F., Hiltunen, T., 2020. Evolution in interacting species alters predator life-history traits, behaviour and morphology in experimental microbial communities. Proceedings of the Royal Society B: Biological Sciences287, 20200652.

[6] Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A., Holmes, S.P., 2016. DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods13, 581–583.

[7] Chaffron, S., Rehrauer, H., Pernthaler, J., Von Mering, C., 2010. A global network of coexisting microbes from environmental and whole-genome sequence data. Genome Research20, 947–959.

[8] Chen, Q.L., Ding, J., Zhu, Y.G., He, J.Z., Hu, H.W., 2020a. Soil bacterial taxonomic diversity is critical to maintaining the plant productivity. Environment International140, 105766.

[9] Chen, Y.J., Leung, P.M., Wood, J.L., Bay, S.K., Hugenholtz, P., Kessler, A.J., Shelley, G., Waite, D.W., Franks, A.E., Cook, P.L.M., Greening, C., 2021c. Metabolic flexibility allows bacterial habitat generalists to become dominant in a frequently disturbed ecosystem. The ISME Journal15, 2986–3004.

[10] Chen, Y.J., Neilson, J.W., Kushwaha, P., Maier, R.M., Barberán, A., 2021b. Life-history strategies of soil microbial communities in an arid ecosystem. The ISME Journal15, 649–657.

[11] Cho, J.C., Giovannoni, S.J., 2004. Cultivation and growth characteristics of a diverse group of oligotrophic marine Gammaproteobacteria. Applied and Environmental Microbiology70, 432–440.

[12] Compant, S., Cambon, M.C., Vacher, C., Mitter, B., Samad, A., Sessitsch, A., 2021. The plant endosphere world–bacterial life within plants. Environmental Microbiology23, 1812–1829.

[13] Dai, T.J., Wen, D.H., Bates, C.T., Wu, L.W., Guo, X., Liu, S., Su, Y.F., Lei, J.S., Zhou, J.Z., Yang, Y.F., 2022. Nutrient supply controls the linkage between species abundance and ecological interactions in marine bacterial communities. Nature Communications13, 175.

[14] de Vries, F.T., Griffiths, R.I., Knight, C.G., Nicolitch, O., Williams, A., 2020. Harnessing rhizosphere microbiomes for drought-resilient crop production. Science368, 270–274.

[15] Fierer, N., Schimel, J.P., 2002. Effects of drying–rewetting frequency on soil carbon and nitrogen transformations. Soil Biology and Biochemistry34, 777–787.

[16] Giovannoni, S.J., 2017. SAR11 bacteria: the most abundant plankton in the oceans. Annual Review of Marine Science9, 231–255.

[17] Gralka, M., Szabo, R., Stocker, R., Cordero, O.X., 2020. Trophic interactions and the drivers of microbial community assembly. Current Biology30, R1176–R1188.

[18] Hamedi, J., Mohammadipanah, F., 2015. Biotechnological application and taxonomical distribution of plant growth promoting actinobacteria. Journal of Industrial Microbiology & Biotechnology42, 157–171.

[19] He, X.G., Xiao, X., Wei, W.W., Li, L.Z., Zhao, Y., Zhang, N., Wang, M.Y., 2024. Soil rare microorganisms mediated the plant cadmium uptake: the central role of protists. Science of the Total Environment908, 168505.

[20] Hernandez, D.J., David, A.S., Menges, E.S., Searcy, C.A., Afkhami, M.E., 2021. Environmental stress destabilizes microbial networks. The ISME Journal15, 1722–1734.

[21] Herren, C.M., McMahon, K.D., 2017. Cohesion: a method for quantifying the connectivity of microbial communities. The ISME Journal11, 2426–2438.

[22] Ho, A., Di Lonardo, D.P., Bodelier, P.L.E., 2017. Revisiting life strategy concepts in environmental microbial ecology. FEMS Microbiology Ecology93, fix006.

[23] Hou, Q., Wang, W.X., Yang, Y., Hu, J., Bian, C.S., Jin, L.P., Li, G.C., Xiong, X.Y., 2020. Rhizosphere microbial diversity and community dynamics during potato cultivation. European Journal of Soil Biology98, 103176.

[24] Kang, J., Peng, Y.F., Xu, W.F., 2022. Crop root responses to drought stress: molecular mechanisms, nutrient regulations, and interactions with microorganisms in the rhizosphere. International Journal of Molecular Sciences23, 9310.

[25] Lauro, F.M., McDougald, D., Thomas, T., Williams, T.J., Egan, S., Rice, S., DeMaere, M.Z., Ting, L., Ertan, H., Johnson, J., Ferriera, S., Lapidus, A., Anderson, I., Kyrpides, N., Munk, A.C., Detter, C., Han, C.S., Brown, M.V., Robb, F.T., Kjelleberg, S., Cavicchioli, R., 2009. The genomic basis of trophic strategy in marine bacteria. Proceedings of the National Academy of Sciences of the United States of America106, 15527–15533.

[26] Li, H., La, S.K., Zhang, X., Gao, L.H., Tian, Y.Q., 2021a. Salt-induced recruitment of specific root-associated bacterial consortium capable of enhancing plant adaptability to salt stress. The ISME Journal15, 2865–2882.

[27] Li, H., Yang, S., Semenov, M.V., Yao, F., Ye, J., Bu, R.C., Ma, R.A., Lin, J.J., Kurganova, I., Wang, X.G., Deng, Y., Kravchenko, I., Jiang, Y., Kuzyakov, Y., 2021b. Temperature sensitivity of SOM decomposition is linked with a K-selected microbial community. Global Change Biology27, 2763–2779.

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

[29] Pandit, S.N., Kolasa, J., Cottenie, K., 2009. Contrasts between habitat generalists and specialists: an empirical extension to the basic metacommunity framework. Ecology90, 2253–2262.

[30] Polz, M.F., Cordero, O.X., 2016. Bacterial evolution: genomics of metabolic trade-offs. Nature Microbiology1, 16181.

[31] R Core Team, 2013. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

[32] Rognes, T., Flouri, T., Nichols, B., Quince, C., Mahé, F., 2016. VSEARCH: a versatile open source tool for metagenomics. PeerJ4, e2584.

[33] Roller, B.R.K., Stoddard, S.F., Schmidt, T.M., 2016. Exploiting rRNA operon copy number to investigate bacterial reproductive strategies. Nature Microbiology1, 16160.

[34] Sanaullah, M., Rumpel, C., Charrier, X., Chabbi, A., 2012. How does drought stress influence the decomposition of plant litter with contrasting quality in a grassland ecosystem? Plant and Soil 352, 277–288.

[35] Santos-Medellín, C., Edwards, J., Liechty, Z., Nguyen, B., Sundaresan, V., 2017. Drought stress results in a compartment-specific restructuring of the rice root-associated microbiomes. MBio8, e00764–17.

[36] Santos-Medellín, C., Liechty, Z., Edwards, J., Nguyen, B., Huang, B.H., Weimer, B.C., Sundaresan, V., 2021. Prolonged drought imparts lasting compositional changes to the rice root microbiome. Nature Plants7, 1065–1077.

[37] Stearns, S.C., 1977. The evolution of life history traits: a critique of the theory and a review of the data. Annual Review of Ecology, Evolution, and Systematics8, 145–171.

[38] Stock, S.C., Köster, M., Dippold, M.A., Nájera, F., Matus, F., Merino, C., Boy, J., Spielvogel, S., Gorbushina, A., Kuzyakov, Y., 2019. Environmental drivers and stoichiometric constraints on enzyme activities in soils from rhizosphere to continental scale. Geoderma337, 973–982.

[39] Stoddard, S.F., Smith, B.J., Hein, R., Roller, B.R.K., Schmidt, T.M., 2015. rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development. Nucleic Acids Research43, D593–D598.

[40] Stone, B.W.G., Dijkstra, P., Finley, B.K., Fitzpatrick, R., Foley, M.M., Hayer, M., Hofmockel, K.S., Koch, B.J., Li, J.H., Liu, X.J.A., Martinez, A., Mau, R.L., Marks, J., Monsaint-Queeney, V., Morrissey, E.M., Propster, J., Pett-Ridge, J., Purcell, A.M., Schwartz, E., Hungate, B.A., 2023. Life history strategies among soil bacteria—dichotomy for few, continuum for many. The ISME Journal17, 611–619.

[41] Tian, P., Razavi, B.S., Zhang, X.C., Wang, Q.K., Blagodatskaya, E., 2020. Microbial growth and enzyme kinetics in rhizosphere hotspots are modulated by soil organics and nutrient availability. Soil Biology and Biochemistry141, 107662.

[42] Trivedi, P., Leach, J.E., Tringe, S.G., Sa, T.M., Singh, B.K., 2020. Plant–microbiome interactions: from community assembly to plant health. Nature Reviews Microbiology18, 607–621.

[43] Van Elsas, J.D., Chiurazzi, M., Mallon, C.A., Elhottovā, D., Krištůfek, V., Salles, J.F., 2012. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proceedings of the National Academy of Sciences of the United States of America109, 1159–1164.

[44] Williams, A., de Vries, F.T., 2020. Plant root exudation under drought: implications for ecosystem functioning. New Phytologist225, 1899–1905.

[45] Xu, L., Dong, Z.B., Chiniquy, D., Pierroz, G., Deng, S.W., Gao, C., Diamond, S., Simmons, T., Wipf, H.M.L., Caddell, D., Varoquaux, N., Madera, M.A., Hutmacher, R., Deutschbauer, A., Dahlberg, J.A., Guerinot, M.L., Purdom, E., Banfield, J.F., Taylor, J.W., Lemaux, P.G., Coleman-Derr, D., 2021. Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics. Nature Communications12, 3209.

[46] Xun, W.B., Li, W., Xiong, W., Ren, Y., Liu, Y.P., Miao, Y.Z., Xu, Z.H., Zhang, N., Shen, Q.R., Zhang, R.F., 2019. Diversity-triggered deterministic bacterial assembly constrains community functions. Nature Communications10, 3833.

[47] Xun, W.B., Liu, Y.P., Li, W., Ren, Y., Xiong, W., Xu, Z.H., Zhang, N., Miao, Y.Z., Shen, Q.R., Zhang, R.F., 2021. Specialized metabolic functions of keystone taxa sustain soil microbiome stability. Microbiome9, 35.

[48] Yan, Y., Kuramae, E.E., de Hollander, M., Klinkhamer, P.G.L., van Veen, J.A., 2017. Functional traits dominate the diversity-related selection of bacterial communities in the rhizosphere. The ISME Journal11, 56–66.

[49] Yang, X.L., Yuan, J., Li, N.N., Franks, A.E., Shentu, J., Luo, Y., Xu, J.M., He, Y., 2021. Loss of microbial diversity does not decrease γ-HCH degradation but increases methanogenesis in flooded paddy soil. Soil Biology and Biochemistry156, 108210.

[50] Yang, Y., Dou, Y.X., Wang, B.R., Xue, Z.J., Wang, Y.Q., An, S.S., Chang, S.X., 2023. Deciphering factors driving soil microbial life-history strategies in restored grasslands. iMeta2, e66.

[51] Yuan, M.M., Guo, X., Wu, L.W., Zhang, Y., Xiao, N.J., Ning, D.L., Shi, Z., Zhou, X.S., Wu, L.Y., Yang, Y.F., Tiedje, J.M., Zhou, J.Z., 2021. Climate warming enhances microbial network complexity and stability. Nature Climate Change11, 343–348.

[52] Zelezniak, A., Andrejev, S., Ponomarova, O., Mende, D.R., Bork, P., Patil, K.R., 2015. Metabolic dependencies drive species co-occurrence in diverse microbial communities. Proceedings of the National Academy of Sciences of the United States of America112, 6449–6454.

RIGHTS & PERMISSIONS

Higher Education Press