Siderophore interactions drive the ability of Pseudomonas spp. consortia to protect tomato against Ralstonia solanacearum

Zhengying Shao , Shaohua Gu , Xiaoni Zhang , Jiao Xue , Tao Yan , Saisai Guo , Thomas Pommier , Alexandre Jousset , Tianjie Yang , Yangchun Xu , Qirong Shen , Zhong Wei

Horticulture Research ›› 2024, Vol. 11 ›› Issue (9) : 186

PDF (213KB)
Horticulture Research ›› 2024, Vol. 11 ›› Issue (9) :186 DOI: 10.1093/hr/uhae186
Articles
research-article
Siderophore interactions drive the ability of Pseudomonas spp. consortia to protect tomato against Ralstonia solanacearum
Author information +
History +
PDF (213KB)

Abstract

The soil-borne bacterial pathogen Ralstonia solanacearum causes significant losses in Solanaceae crop production worldwide, including tomato, potato, and eggplant. To efficiently prevent outbreaks, it is essential to understand the complex interactions between pathogens and the microbiome. One promising mechanism for enhancing microbiome functionality is siderophore-mediated competition, which is shaped by the low iron availability in the rhizosphere. This study explores the critical role of iron competition in determining microbiome functionality and its potential for designing high-performance microbiome engineering strategies. We investigated the impact of siderophore-mediated interactions on the efficacy of Pseudomonas spp. consortia in suppressing R. solanacearum, both in vitro and in vivo. Our findings show that siderophore production significantly enhances the inhibitory effects of Pseudomonas strains on pathogen growth, while other metabolites are less effective under iron-limited conditions. Moreover, siderophores play a crucial role in shaping interactions within the consortia, ultimately determining the level of protection against bacterial wilt disease. This study highlights the key role of siderophores in mediating consortium interactions and their impact on tomato health. Our results also emphasize the limited efficacy of other secondary metabolites in iron-limited environments, underscoring the importance of siderophore-mediated competition in maintaining tomato health and suppressing disease.

Cite this article

Download citation ▾
Zhengying Shao, Shaohua Gu, Xiaoni Zhang, Jiao Xue, Tao Yan, Saisai Guo, Thomas Pommier, Alexandre Jousset, Tianjie Yang, Yangchun Xu, Qirong Shen, Zhong Wei. Siderophore interactions drive the ability of Pseudomonas spp. consortia to protect tomato against Ralstonia solanacearum. Horticulture Research, 2024, 11 (9) : 186 DOI:10.1093/hr/uhae186

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This research was funded by the National Natural Science Foundation of China (42090060, 42325704, 42277113, and 42107140), the Fundamental Research Funds for the Central Universities (KYT2024001), the Natural Science Foundation of Jiangsu Province (BK20230102), the Jiangsu Agricultural Science and Technology Innovation Fund (CX(22)1004, SCX(24)3511) and the Jiangsu Carbon Peak & Carbon Neutrality Science and Technology Innovation Special Fund (BE2022423).

Author contributions

Z.W., Y.X., and Q.S.: conceptualization and project administration. Z.S., S.Gu, and Z.W.: methodology, software, formal analysis, visualization, and writing original draft. X.Z., J.X., T.Y., S.Guo, and Z.W.: resources, investigation, and data curation. T.P., A.J., Z.W., and T.Y.: writing - review and editing.

Data availability

The data for this article are available in the article or in its supplementary material.

Conflict of interest

The authors declare no conflict of interest.

Supplementary data

Supplementary data are available at Horticulture Research online.

References

[1]

Wang Z, Luo W, Cheng S. et al. Ralstonia solanacearum - a soil borne hidden enemy of plants: research development in management strategies, their action mechanism and challenges. Front Plant Sci. 2023; 14:1141902

[2]

An Y, Zhang M. Advances in understanding dynamic host-microbe interactions during Ralstonia solanacearum infection and their implications for crop disease resistance. New Crops. 2024; 1:100014

[3]

Ahmed W, Yang J, Tan Y. et al. Ralstonia solanacearum, a deadly pathogen: revisiting the bacterial wilt biocontrol practices in tobacco and other Solanaceae. Rhizosphere. 2022; 21:100479

[4]

Jangir M, Pathak R, Sharma S. et al. Biocontrol mechanisms of Bacillus sp., isolated from tomato rhizosphere, against Fusarium oxysporum f. sp. lycopersici. Biol Control. 2018; 123:60-70

[5]

Trivedi P, Leach JE, Tringe SG. et al. Plant-microbiome interactions: from community assembly to plant health. Nat Rev Microbiol. 2020; 18:607-21

[6]

Hunjan MS, Thakur A, Singh PP. Identification and characterization of Pseudomonas fluorescens strains effective against Xanthomonas oryzae pv. oryzae causing bacterial blight of rice in Punjab. India. J Appl Nat Sci. 2017; 9:253-61

[7]

Barahona E, Navazo A, Garrido-Sanz D. et al. Pseudomonas fluorescens F113 can produce a second flagellar apparatus, which is important for plant root colonization. Front Microbiol. 2016; 7:1471

[8]

Backer R, Rokem JS, Ilangumaran G. et al. Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front Plant Sci. 2018; 9:1473

[9]

Köhl J, Kolnaar R, Ravensberg WJ. Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Front Plant Sci. 2019; 10:845

[10]

Xu Z, Wang M, Du J. et al. Isolation of Burkholderia sp. HQB-1, a promising biocontrol bacteria to protect banana against Fusarium wilt through phenazine-1-carboxylic acid secretion. Front Microbiol. 2020; 11:605152

[11]

Jung BK, Hong S-J, Park G-S. et al. Isolation of Burkholderia cepacia JBK9 with plant growth-promoting activity while producing pyrrolnitrin antagonistic to plant fungal diseases. Appl Biol Chem. 2018; 61:173-80

[12]

Feng S, Jin L, Tang S. et al. Combination of rhizosphere bacteria isolated from resistant potato plants for biocontrol of potato late blight. Pest Manag Sci. 2022; 78:166-76

[13]

Gu S, Wei Z, Shao Z. et al. Competition for iron drives phytopathogen control by natural rhizosphere microbiomes. Nat Microbiol. 2020; 5:1002-10

[14]

Wei Z, Yang T, Friman VP. et al. Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nat Commun. 2015; 6:8413

[15]

Andrews SC, Robinson AK, Rodríguez-Quiñones F. Bacterial iron homeostasis. FEMS Microbiol Rev. 2003; 27:215-37

[16]

Robin A, Vansuyt G, Hinsinger P. et al. Iron dynamics in the rhizosphere:consequences for plant health and nutrition. In: Advances in Agronomy. Vol. 99. 2008,183-225

[17]

Maurice PA, Vierkorn MA, Hersman LE. et al. Enhancement of kaolinite dissolution by an aerobic Pseudomonas mendocina bacterium. Geomicrobiol J. 2001; 18:21-35

[18]

Saha M, Sarkar S, Sarkar B. et al. Microbial siderophores and their potential applications: a review. Environ Sci Pollut Res Int. 2016; 23:3984-99

[19]

Arya N, Rana A, Rajwar A. et al. Biocontrol efficacy of siderophore producing indigenous Pseudomonas strains against Fusarium wilt in tomato. Nat Acad Sci Lett. 2018; 41:133-6

[20]

Sasirekha B, Srividya S. Siderophore production by Pseudomonas aeruginosa FP6, a biocontrol strain for Rhizoctonia solani and Colletotrichum gloeosporioides causing diseases in chilli. Agric Nat Resour. 2016; 50:250-6

[21]

Schalk IJ, Guillon L. Pyoverdine biosynthesis and secretion in Pseudomonas aeruginosa: implications for metal homeostasis. Environ Microbiol. 2013; 15:1661-73

[22]

Meyer JM, Geoffroy VA, Baida N. et al. Siderophore typing, a powerful tool for the identification of fluorescent and non-fluorescent pseudomonads. Appl Environ Microbiol. 2002; 68:2745-53

[23]

Mercado-Blanco J. Pseudomonas strains that exert biocontrol of plant pathogens. In: Ramos JL, Goldberg JB, Filloux A,eds. Pseudomonas:New Aspects of Pseudomonas Biology. Dordrecht: Springer, 2015,121-72

[24]

Meyer J-M, Gruffaz C, Raharinosy V. et al. Siderotyping of fluorescent Pseudomonas: molecular mass determination by mass spectrometry as a powerful pyoverdine siderotyping method. Biometals. 2008; 21:259-71

[25]

Jeong G-J, Khan F, Tabassum N. et al. Roles of Pseudomonas aeruginosa siderophores in interaction with prokaryotic and eukaryotic organisms. Res Microbiol. 2024;104211

[26]

Deb CR, Tatung M. Siderophore producing bacteria as biocontrol agent against phytopathogens for a better environment: a review. S Afr J Bot. 2024; 165:153-62

[27]

Gu S, Shao Z, Qu Z. et al. Siderophore-receptor coevolution analysis reveals habitat- and pathogen-specific bacterial iron interaction networks. bioRxiv. 2023

[28]

Kramer J, Ozkaya O, Kummerli R. Bacterial siderophores in community and host interactions. Nat Rev Microbiol. 2020; 18:152-63

[29]

Stubbendieck RM, Vargas-Bautista C, Straight PD. Bacterial communities: interactions to scale. Front Microbiol. 2016; 7:1234

[30]

Li M, Wei Z, Wang J. et al. Facilitation promotes invasions in plant-associated microbial communities. Ecol Lett. 2019; 22:149-58

[31]

de los Santos-Villalobos S, Barrera-Galicia GC, Miranda-Salcedo MA. et al. Burkholderia cepacia XXVI siderophore with biocontrol capacity against Colletotrichum gloeosporioides. World J Microbiol Biotechnol. 2012; 28:2615-23

[32]

Yu X, Ai C, Xin L. et al. The siderophore-producing bacterium, Bacillus subtilis CAS15, has a biocontrol effect on Fusarium wilt and promotes the growth of pepper. Eur J Soil Biol. 2011; 47:138-45

[33]

Gu S, Yang T, Shao Z. et al. Siderophore-mediated interactions determine the disease suppressiveness of microbial consortia. mSystems. 2020; 5:e00811-9

[34]

Haas D, Keel C. Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annu Rev Phytopathol. 2003; 41:117-53

[35]

Hu J, Wei Z, Friman VP. et al. Probiotic diversity enhances rhizosphere microbiome function and plant disease suppression. MBio. 2016; 7:1110-28

[36]

Butaite E, Baumgartner M, Wyder S. et al. Siderophore cheating and cheating resistance shape competition for iron in soil and freshwater Pseudomonas communities. Nat Commun. 2017; 8:414

[37]

Höfte M, Buysens S, Koedam N. et al. Zinc affects siderophore-mediated high affinity iron uptake systems in the rhizosphere Pseudomonas aeruginosa 7NSK2. Biometals. 1993; 6:85-91

[38]

Zhou T, Chen D, Li C. et al. Isolation and characterization of Pseudomonas brassicacearum J12 as an antagonist against Ralstonia solanacearum and identification of its antimicrobial components. Microbiol Res. 2012; 167:388-94

[39]

Jousset A, Bonkowski M. The model predator Acanthamoeba castellanii induces the production of 2,4,DAPG by the biocontrol strain Pseudomonas fluorescens Q2-87. Soil Biol Biochem. 2010; 42:1647-9

[40]

Peng J, Chen G, Xu X. et al. Iron facilitates the RetS-Gac-Rsm cascade to inversely regulate protease IV (piv) expression via the sigma factor PvdS in Pseudomonas aeruginosa. Environ Microbiol. 2020; 22:5402-13

[41]

Sindhu SS, Rakshiya YS, Sahu G. Biological control of soilborne plant pathogens with rhizosphere bacteria. Pest Technol. 2009; 3:10-21

[42]

Santoyo G, Guzmán-Guzmán P, Parra-Cota FI. et al. Plant growth stimulation by microbial consortia. Agronomy. 2021; 11:219

[43]

West SA, Buckling A. Cooperation, virulence and siderophore production in bacterial parasites. Proc Biol Sci. 2003; 270:37-44

[44]

Joshi F, Archana G, Desai A. Siderophore cross-utilization amongst rhizospheric bacteria and the role of their differential affinities for Fe3+ on growth stimulation under iron-limited conditions. Curr Microbiol. 2006; 53:141-7

[45]

Hibbing ME, Fuqua C, Parsek MR. et al. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol. 2010; 8:15-25

[46]

Sheng MM, Jia HK, Zhang GY. et al.Siderophore production by rhizosphere biological control bacteria Brevibacillus brevis GZDF3 of Pinellia ternata and its antifungal effects on Candida albicans. J Microbiol Methods. 2020; 30:689-99

[47]

Hammer E, Kneifel H, Hofmann K. et al. Enhanced excretion of intermediates of aromatic amino acid catabolism during chlorophenol degradation due to nutrient limitation in the yeast Candida maltosa. J Basic Microbiol. 1996; 36:239-43

[48]

Graham AI, Hunt S, Stokes SL. et al. Severe zinc depletion of Escherichia coli: roles for high affinity zinc binding by ZinT, zinc transport and zinc-independent proteins. J Biol Chem. 2009; 284:18377-89

[49]

Droby S, Wisniewski M, Teixidó N. et al. The science, development, and commercialization of postharvest biocontrol products. Postharvest Biol Technol. 2016; 122:22-9

[50]

Haggag WM, Nofal M. Improving the biological control of Botryodiplodia disease on some Annona cultivars using single or multi-bioagents in Egypt. Biol Control. 2006; 38:341-9

[51]

Guetsky R, Shtienberg D, Elad Y. et al. Combining biocontrol agents to reduce the variability of biological control. Phytopathology. 2001; 91:621-7

[52]

Ratzke C, Barrere J, Gore J. Strength of species interactions determines biodiversity and stability in microbial communities. Nat Ecol Evol. 2020; 4:376-83

[53]

Bahram M, Netherway T, Hildebrand F. et al. Plant nutrient-acquisition strategies drive topsoil microbiome structure and function. New Phytol. 2020; 227:1189-99

[54]

Li M, Pommier T, Yin Y. et al. Resource availability drives bacteria community resistance to pathogen invasion via altering bacterial pairwise interactions. Environ Microbiol. 2022; 24:5680-9

[55]

Sun X, Zhang C, Bei S. et al. High bacterial diversity and siderophore-producing bacteria collectively suppress Fusarium oxysporum in maize/faba bean intercropping. Front Microbiol. 2022; 13:972587

[56]

Sharifi R, Ahmadzadeh M, Sharifi-Tehrani A. et al. Pyoverdine production in Pseudomonas fluorescens UTPF5 and its association with suppression of common bean damping off caused by Rhizoctonia solani ( Kühn). J Plant Protect Res. 2010; 50:72-8

[57]

Devi KK, Kothamasi D. Pseudomonas fluorescens CHA0 can kill subterranean termite Odontotermes obesus by inhibiting cytochrome c oxidase of the termite respiratory chain. FEMS Microbiol Lett. 2009; 300:195-200

[58]

Pillonel C, Meyer T. Effect of phenylpyrroles on glycerol accumulation and protein kinase activity of Neurospora crassa. Pestic Sci. 1997; 49:229-36

[59]

Kaplan J, McVey Ward D, Crisp RJ. et al. Iron-dependent metabolic remodeling in S. cerevisiae. Biochim Biophys Acta. 2006; 1763:646-51

[60]

Shimizu K. Regulation systems of bacteria such as Escherichia coli in response to nutrient limitation and environmental stresses. Metabolites. 2013; 4:1-35

[61]

Bykowski T, van der Ploeg JR, Iwanicka-Nowicka R. et al. The switch from inorganic to organic sulphur assimilation in Escherichia coli: adenosine 5′-phosphosulphate (APS) as a signalling molecule for sulphate excess. Mol Microbiol. 2002; 43:1347-58

[62]

Zhang Q, Kong X, Li S. et al. Antibiotics of Pseudomonas protegens FD6 are essential for biocontrol activity. Australas Plant Pathol. 2020; 49:307-17

[63]

Soares EV. Perspective on the biotechnological production of bacterial siderophores and their use. Appl Microbiol Biotechnol. 2022; 106:3985-4004

[64]

Jousset A, Schulz W, Scheu S. et al. Intraspecific genotypic richness and relatedness predict the invasibility of microbial communities. ISME J. 2011; 5:1108-14

[65]

Zhu J, Wang J, Chen Y-P. et al. Quantitative proteomics and phosphoproteomics elucidate the molecular mechanism of nanostructured TiO2-stimulated biofilm formation. J Hazard Mater. 2022; 432:128709

[66]

Wei Z, Yang X, Yin S. et al. Efficacy of Bacillus-fortified organic fertiliser in controlling bacterial wilt of tomato in the field. Appl Soil Ecol. 2011; 48:152-9

[67]

Schwyn B, Neilands J. Universal chemical assay for the detection and determination of siderophores. Anal Biochem. 1987; 160:47-56

[68]

Bangera MG, Thomashow LS. Identification and characterization of a gene cluster for synthesis of the polyketide antibiotic 2,4-diacetylphloroglucinol from Pseudomonas fluorescens Q2-87. J Bacteriol. 1999; 181:3155-63

[69]

Achkar J, Xian M, Zhao H. et al. Biosynthesis of phloroglucinol. J Am Chem Soc. 2005; 127:5332-3

[70]

Kidarsa TA, Goebel NC, Zabriskie TM. et al. Phloroglucinol mediates cross-talk between the pyoluteorin and 2,4-diacetylphloroglucinol biosynthetic pathways in Pseudomonas fluorescens Pf-5. Mol Microbiol. 2011; 81:395-414

[71]

Almario J, Moënne-Loccoz Y, Muller D. Monitoring of the relation between 2,4-diacetylphloroglucinol-producing Pseudomonas and Thielaviopsis basicola populations by real-time PCR in tobacco black root-rot suppressive and conducive soils. Soil Biol Biochem. 2013; 57:144-55

[72]

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 2001; 25:402-8

[73]

Alqarni B, Colley B, Klebensberger J. et al. Expression stability of 13 housekeeping genes during carbon starvation of Pseudomonas aeruginosa. J Microbiol Methods. 2016; 127:182-7

[74]

Jeger M, Viljanen-Rollinson S. The use of the area under the disease-progress curve (AUDPC) to assess quantitative disease resistance in crop cultivars. Theor Appl Genet. 2001; 102:32-40

[75]

Eisenhauer N, Bowker MA, Grace JB. et al. From patterns to causal understanding: structural equation modeling (SEM) in soil ecology. Pedobiologia. 2015; 58:65-72

PDF (213KB)

84

Accesses

0

Citation

Detail

Sections
Recommended

/