Abstract
Soil bacteria are widely recognized for their roles in nutrient cycling, such as for nitrogen and phosphorus, and for promoting soil health. However, the relationship between soil bacteria and the availability of calcium, magnesium, iron, manganese, copper and zinc under different climatic conditions in orchard systems remains poorly understood. Here, we explored the relationship between soil bacteria and metal nutrient availability and uptake by apple trees based on 36 soil samples from three climate zones that span the major apple-producing areas in China. The results indicated that six phyla (e.g., Acidobacteria, Actinobacteria, Chloroflexi, Gemmatimonadetes, Nitrospirae, and Proteobacteria) in the soil bacterial communities were positively related to the metal nutrients availability, especially to calcium (16 OTUs) and magnesium (19 OTUs). At the class level, Alphaproteobacteria improved the availability of calcium, magnesium, iron, manganese and copper, while Actinobacteria improved the availability of zinc and altered absorption by the roots and the contents in leaves. We found that the underground bacterial community diversity was determined by climatic conditions and soil properties, which altered the effect of bacteria on soil metal nutrients availability, and led to differences of nutritional content in the aboveground plant portions. Therefore, soil bacteria played a central role in this process for sustainable development in apple orchard systems.
Similar content being viewed by others
References
Adeleke R, Nwangburuka C, Oboirien B (2017) Origins, roles and fate of organic acids in soils: a review. S Afr J Bot 108:393–406. https://doi.org/10.1016/j.sajb.2016.09.002
Balland-Bolou-Bi C et al (2019) Impact of microbial activity on the mobility of metallic elements (Fe, Al and Hg) in tropical soils. Geoderma 334:146–154. https://doi.org/10.1016/j.geoderma.2018.07.044
Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511. https://doi.org/10.1038/nature13855
Bates ST, Berg-Lyons D, Caporaso JG, Walters WA, Knight R, Fierer N (2011) Examining the global distribution of dominant archaeal populations in soil. ISME J 5:908–917. https://doi.org/10.1038/ismej.2010.171
Begg SL (2019) The role of metal ions in the virulence and viability of bacterial pathogens. Biochem Soc Trans 47:77–87. https://doi.org/10.1042/BST20180275
Bettger WJ, O'Dell BL (1981) A critical physiological role of zinc in the structure and function of biomembranes. Life Sci 28:1425–1438. https://doi.org/10.1016/0024-3205(81)90374-X
Biggss AR, Peck GM (2015) Managing bitter pit in 'Honeycrisp' apples grown in the Mid-Atlantic United States with foliar-applied calcium chloride and some alternatives. Horttechnology 25:385–391. https://doi.org/10.21273/HORTTECH.25.3.385
Braud A, Hannauer M, Mislin GL, Schalk IJ (2009) The Pseudomonas aeruginosa pyochelin-iron uptake pathway and its metal specificity. J Bacteriol 191:3517–3525. https://doi.org/10.1128/JB.00010-09
Bundeleva IA, Shirokova LS, Bénézeth P, Pokrovsky OS, Kompantseva EI, Balor S (2012) Calcium carbonate precipitation by anoxygenic phototrophic bacteria. Chem Geol 291:116–131. https://doi.org/10.1016/j.chemgeo.2011.10.003
Canarini A, Carrillo Y, Mariotte P, Ingram L, Dijkstra FA (2016) Soil microbial community resistance to drought and links to C stabilization in an Australian grassland. Soil Biol Biochem 103:171–180. https://doi.org/10.1016/j.soilbio.2016.08.024
Chen XD, Dunfield KE, Fraser TD, Wakelin SA, Richardson AE, Condron LM (2020) Soil biodiversity and biogeochemical function in managed ecosystems. Soil Res 58:1–20. https://doi.org/10.1071/SR19067
Dimkpa CO, Bindraban PS (2016) Fortification of micronutrients for efficient agronomic production: a review. Agron Sustain Dev. https://doi.org/10.1007/s13593-015-0346-6
Edwards J et al (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci USA 112:E911–E920. https://doi.org/10.1073/pnas.1414592112
Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631. https://doi.org/10.1073/pnas.0507535103
Geisen S, Wall DH, van der Putten WH (2019) Challenges and opportunities for soil biodiversity in the anthropocene. Curr Biol 29:R1036–R1044. https://doi.org/10.1016/j.cub.2019.08.007
Gerard E et al (2018) Key role of Alphaproteobacteria and Cyanobacteria in the formation of stromatolites of Lake Dziani Dzaha (Mayotte, Western Indian Ocean). Front Microbiol 9:796. https://doi.org/10.3389/fmicb.2018.00796
Goberna M, Navarro-Cano JA, Valiente-Banuet A, Garcia C, Verdu M (2014) Abiotic stress tolerance and competition-related traits underlie phylogenetic clustering in soil bacterial communities. Ecol Lett 17:1191–1201. https://doi.org/10.1111/ele.12341
Jansson JK, Hofmockel KS (2020) Soil microbiomes and climate change. Nat Rev Microbiol 18:35–46. https://doi.org/10.1038/s41579-019-0265-7
Kong J, Dong Y, Xu L, Liu S, Bai X (2013) Role of exogenous nitric oxide in alleviating iron deficiency-induced peanut chlorosis on calcareous soil. J Plant Interact 9:450–459. https://doi.org/10.1080/17429145.2013.853327
Levin AG, Yermiyahu U, Doron I, Shtienberg D (2019) The role of calcium concentration in the endocarp wall of apple fruit in the development of core rot. Crop Prot 120:67–74. https://doi.org/10.1016/j.cropro.2019.02.023
Li X, Zhang J, Gai J, Cai X, Christie P, Li X (2015) Contribution of arbuscular mycorrhizal fungi of sedges to soil aggregation along an altitudinal alpine grassland gradient on the Tibetan Plateau. Environ Microbiol 17:2841–2857. https://doi.org/10.1111/1462-2920.12792
Li H et al (2016) Responses of soil bacterial communities to nitrogen deposition and precipitation increment are closely linked with aboveground community variation. Microb Ecol 71:974–989. https://doi.org/10.1007/s00248-016-0730-z
Liang Y et al (2015) Long-term soil transplant simulating climate change with latitude significantly alters microbial temporal turnover. ISME J 9:2561–2572. https://doi.org/10.1038/ismej.2015.78
Ma S, Ding Z, Li P (2017) Maize network analysis revealed gene modules involved in development, nutrients utilization, metabolism, and stress response. BMC Plant Biol 17:131. https://doi.org/10.1186/s12870-017-1077-4
Malik AA, Martiny JBH, Brodie EL, Martiny AC, Treseder KK, Allison SD (2020) Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change. ISME J 14:1–9. https://doi.org/10.1038/s41396-019-0510-0
Mau RL et al (2015) Linking soil bacterial biodiversity and soil carbon stability. ISME J 9:1477–1480. https://doi.org/10.1038/ismej.2014.205
Murphy DV, Cookson WR, Braimbridge M, Marschner P, Jones DL, Stockdale EA, Abbott LK (2011) Relationships between soil organic matter and the soil microbial biomass (size, functional diversity, and community structure) in crop and pasture systems in a semi-arid environment. Soil Res 49:582–594. https://doi.org/10.1071/SR11203
Nielsen KE, Irizar A, Nielsen LP, Kristiansen SM, Damgaard C, Holmstrup M, Petersen AR, Strandberg M (2017) In situ measurements reveal extremely low pH in soil. Soil Biol Biochem 115:63–65. https://doi.org/10.1016/j.soilbio.2017.08.003
Orland C, Emilson EJS, Basiliko N, Mykytczuk NCS, Gunn JM, Tanentzap AJ (2019) Microbiome functioning depends on individual and interactive effects of the environment and community structure. ISME J 13:1–11. https://doi.org/10.1038/s41396-018-0230-x
Osburn ED, McBride SG, Aylward FO, Badgley BD, Strahm BD, Knoepp JD, Barrett JE (2019) Soil bacterial and fungal communities exhibit distinct long-term responses to disturbance in temperate forests. Front Microbiol. https://doi.org/10.3389/fmicb.2019.02872
Parmar P, Sindhu SS (2019) The novel and efficient method for isolating potassium solubilizing bacteria from rhizosphere soil. Geomicrobiol J 36:130–136. https://doi.org/10.1080/01490451.2018.1514442
Pokharel R, Gerrits R, Schuessler JA, Frings PJ, Sobotka R, Gorbushina AA, von Blanckenburg F (2018) Magnesium stable isotope fractionation on a cellular level explored by Cyanobacteria and Black Fungi with implications for higher plants. Environ Sci Technol 52:12216–12224. https://doi.org/10.1021/acs.est.8b02238
Rashid MI, Mujawar LH, Shahzad T, Almeelbi T, Ismail IMI, Oves M (2016) Bacteria and fungi can contribute to nutrients bioavailability and aggregate formation in degraded soils. Microbiol Res 183:26–41. https://doi.org/10.1016/j.micres.2015.11.007
Ren C et al (2016) Linkages of C:N: P stoichiometry and bacterial community in soil following afforestation of former farmland. For Ecol Manag 376:59–66. https://doi.org/10.1016/j.foreco.2016.06.004
Revillini D, Gehring CA, Johnson NC (2016) The role of locally adapted mycorrhizas and rhizobacteria in plant-soil feedback systems. Funct Ecol 30:1086–1098. https://doi.org/10.1111/1365-2435.12668
Ribbons RR, Levy-Booth DJ, Masse J, Grayston SJ, McDonald MA, Vesterdal L, Prescott CE (2016) Linking microbial communities, functional genes and nitrogen-cycling processes in forest floors under four tree species. Soil Biol Biochem 103:181–191. https://doi.org/10.1016/j.soilbio.2016.07.024
Romheld V, Marschner H (1986) Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol 80:175–180. https://doi.org/10.1104/pp.80.1.175
Schalk IJ, Hannauer M, Braud A (2011) New roles for bacterial siderophores in metal transport and tolerance. Environ Microbiol 13:2844–2854. https://doi.org/10.1111/j.1462-2920.2011.02556.x
Shen JP, Zhang LM, Guo JF, Ray JL, He JZ (2010) Impact of long-term fertilization practices on the abundance and composition of soil bacterial communities in Northeast China. Appl Soil Ecol 46:119–124. https://doi.org/10.1016/j.apsoil.2010.06.015
Sokri SM, Babalar M, Barker AV, Lesani H, Asgari MA (2015) Fruit quality and nitrogen, potassium, and calcium content of apple as influenced by nitrate:ammonium ratios in tree nutrition. J Plant Nutr 38:1619–1627. https://doi.org/10.1080/01904167.2014.964364
Sun L et al (2016) Alteration of the soil bacterial community during parent material maturation driven by different fertilization treatments. Soil Biol Biochem 96:207–215. https://doi.org/10.1016/j.soilbio.2016.02.011
Suo GD, Xie YS, Zhang Y, Luo H (2019) Long-term effects of different surface mulching techniques on soil water and fruit yield in an apple orchard on the Loess Plateau of China. Sci Hortic 246:643–651. https://doi.org/10.1016/j.scienta.2018.11.028
Trap J, Bonkowski M, Plassard C, Villenave C, Blanchart E (2016) Ecological importance of soil bacterivores for ecosystem functions. Plant Soil 398:1–24. https://doi.org/10.1007/s11104-015-2671-6
Vieira de Souza BS, Sousa Silva KC, Alves Parente AF, Borges CL, Paccez JD, Pereira M, de Almeida Soares CM, Giambiagi-deMarval M, Silva-Bailao MG, Parente-Rocha JA (2019) The influence of pH on Staphylococcus saprophyticus iron metabolism and the production of siderophores. Microbes Infect 21:456–463. https://doi.org/10.1016/j.micinf.2019.04.008
Viets FG (1962) Micronutrient availability: chemistry and availability of micronutrients in soils. J Agric Food Chem 10:174–178. https://doi.org/10.1021/Jf60121a004
Wang D, Fierke CA (2013) The BaeSR regulon is involved in defense against zinc toxicity in E. coli. Metallomics 5:372–383. https://doi.org/10.1039/c3mt20217h
Wang SP, Loreau M (2016) Biodiversity and ecosystem stability across scales in metacommunities. Ecol Lett 19:510–518. https://doi.org/10.1111/ele.12582
Wang GY, Zhang XZ, Wang Y, Xu XF, Han ZH (2015) Key minerals influencing apple quality in Chinese orchard identified by nutritional diagnosis of leaf and soil analysis. J Integr Agric 14:864–874. https://doi.org/10.1016/s2095-3119(14)60877-7
Wang N, Joost W, Zhang FS (2016) Towards sustainable intensification of apple production in China-Yield gaps and nutrient use efficiency in apple farming systems. J Integr Agric 15:716–725. https://doi.org/10.1016/S2095-3119(15)61099-1
Weidner S, Koller R, Latz E, Kowalchuk G, Bonkowski M, Scheu S, Jousset A (2015) Bacterial diversity amplifies nutrient-based plant-soil feedbacks. Funct Ecol 29:1341–1349. https://doi.org/10.1111/1365-2435.12445
Wilson GW, Rice CW, Rillig MC, Springer A, Hartnett DC (2009) Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments. Ecol Lett 12:452–461. https://doi.org/10.1111/j.1461-0248.2009.01303.x
Xiao M, Wu F (2014) A review of environmental characteristics and effects of low-molecular weight organic acids in the surface ecosystem. J Environ Sci 26:935–954. https://doi.org/10.1016/s1001-0742(13)60570-7
Zhang C, Liu GB, Xue S, Wang GL (2016) Soil bacterial community dynamics reflect changes in plant community and soil properties during the secondary succession of abandoned farmland in the Loess Plateau. Soil Biol Biochem 97:40–49. https://doi.org/10.1016/j.soilbio.2016.02.013
Zhang D et al (2018) Linking plant ecological stoichiometry with soil nutrient and bacterial communities in apple orchards. Appl Soil Ecol 126:1–10. https://doi.org/10.1016/j.apsoil.2017.12.017
Zhang M et al (2017) Loss of soil microbial diversity may increase insecticide uptake by crop. Agr Ecosyst Environ 240:84–91. https://doi.org/10.1016/j.agee.2017.02.010
Zheng W, Zhao Z, Gong Q, Zhai B, Li Z (2018) Effects of cover crop in an apple orchard on microbial community composition, networks, and potential genes involved with degradation of crop residues in soil. Biol Fertil Soils 54:743–759. https://doi.org/10.1007/s00374-018-1298-1
Zhong WH, Cai ZC (2007) Long-term effects of inorganic fertilizers on microbial biomass and community functional diversity in a paddy soil derived from quaternary red clay. Appl Soil Ecol 36:84–91. https://doi.org/10.1016/j.apsoil.2006.12.001
Acknowledgements
This work was funded by the National key research and development program (2016YFD0201100).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that there is no conflict of interests regarding the publication of this article.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Dong Zhang and Shunfeng Ge have contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhang, D., Ge, S., Wang, C. et al. The relationship between soil bacteria and metal nutrient availability for uptake of apple trees in Chinese orchards. Plant Growth Regul 92, 181–193 (2020). https://doi.org/10.1007/s10725-020-00629-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-020-00629-w