Survival of a microbial inoculant in soil after recurrent inoculations.
Nitrogen cycle
PGPR
Recurrent inoculation
Soil bacteria
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
20 Feb 2024
20 Feb 2024
Historique:
received:
31
10
2023
accepted:
08
02
2024
medline:
21
2
2024
pubmed:
21
2
2024
entrez:
20
2
2024
Statut:
epublish
Résumé
Microbial inoculants are attracting growing interest in agriculture, but their efficacy remains unreliable in relation to their poor survival, partly due to the competition with the soil resident community. We hypothesised that recurrent inoculation could gradually alleviate this competition and improve the survival of the inoculant while increasing its impact on the resident bacterial community. We tested the effectiveness of such strategy with four inoculation sequences of Pseudomonas fluorescens strain B177 in soil microcosms with increasing number and frequency of inoculation, compared to a non-inoculated control. Each sequence was carried out at two inoculation densities (10
Identifiants
pubmed: 38378706
doi: 10.1038/s41598-024-54069-x
pii: 10.1038/s41598-024-54069-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
4177Subventions
Organisme : Agence Nationale de la Recherche
ID : ANR-20-CE02-0014
Informations de copyright
© 2024. The Author(s).
Références
Sebilo, M., Mayer, B., Nicolardot, B., Pinay, G. & Mariotti, A. Long-term fate of nitrate fertilizer in agricultural soils. Proc. Natl. Acad. Sci. 110, 18185–18189 (2013).
pubmed: 24145428
pmcid: 3831475
doi: 10.1073/pnas.1305372110
Liess, M. et al. Pesticides are the dominant stressors for vulnerable insects in lowland streams. Water Res. 201, 117262 (2021).
pubmed: 34118650
doi: 10.1016/j.watres.2021.117262
Schulz, R., Bub, S., Petschick, L. L., Stehle, S. & Wolfram, J. Applied pesticide toxicity shifts toward plants and invertebrates, even in GM crops. Science 372, 81–84 (2021).
pubmed: 33795455
doi: 10.1126/science.abe1148
Schütz, L. et al. Improving crop yield and nutrient use efficiency via biofertilization—a global meta-analysis. Front. Plant Sci. 8, 2204 (2018).
pubmed: 29375594
pmcid: 5770357
doi: 10.3389/fpls.2017.02204
Porter, S. S. et al. Beneficial microbes ameliorate abiotic and biotic sources of stress on plants. Funct. Ecol. 34, 2075–2086 (2020).
doi: 10.1111/1365-2435.13499
O’Brien, P. A. Biological control of plant diseases. Austral. Plant Pathol. 46, 293–304 (2017).
doi: 10.1007/s13313-017-0481-4
Liu, X., LeRoux, X. & Salles, J. F. The legacy of microbial inoculants in agroecosystems and potential for tackling climate change challenges. iScience 25, 103821 (2022).
pubmed: 35243218
pmcid: 8867051
doi: 10.1016/j.isci.2022.103821
Santos, M. S., Nogueira, M. A. & Hungria, M. Microbial inoculants: Reviewing the past, discussing the present and previewing an outstanding future for the use of beneficial bacteria in agriculture. AMB Express 9, 205 (2019).
pubmed: 31865554
pmcid: 6925611
doi: 10.1186/s13568-019-0932-0
Waltz, E. A new crop of microbe startups raises big bucks, takes on the establishment. Nat. Biotechnol. 35, 1120–1122 (2017).
pubmed: 29220026
doi: 10.1038/nbt1217-1120
Kaminsky, L. M., Trexler, R. V., Malik, R. J., Hockett, K. L. & Bell, T. H. The inherent conflicts in developing soil microbial inoculants. Trends Biotechnol. https://doi.org/10.1016/j.tibtech.2018.11.011 (2019).
doi: 10.1016/j.tibtech.2018.11.011
pubmed: 31103070
Parnell, J. J. et al. From the lab to the farm: An industrial perspective of plant beneficial microorganisms. Front. Plant Sci. 7, 25 (2016).
doi: 10.3389/fpls.2016.01110
Fischer, S. E., Jofré, E. C., Cordero, P. V., GutiérrezMañero, F. J. & Mori, G. B. Survival of native Pseudomonas in soil and wheat rhizosphere and antagonist activity against plant pathogenic fungi. Antonie van Leeuwenhoek 97, 241–251 (2010).
pubmed: 20020326
doi: 10.1007/s10482-009-9405-9
Sharma, R. et al. Survival, efficacy and rhizospheric effects of bacterial inoculants on Cajanus cajan. Agric. Ecosyst. Environ. 240, 244–252 (2017).
doi: 10.1016/j.agee.2017.02.018
Mallon, C. A., van Elsas, J. D. & Salles, J. F. Microbial invasions: The process, patterns, and mechanisms. Trends Microbiol. 23, 719–729 (2015).
pubmed: 26439296
doi: 10.1016/j.tim.2015.07.013
Schreiter, S. et al. Soil type-dependent effects of a potential biocontrol inoculant on indigenous bacterial communities in the rhizosphere of field-grown lettuce. FEMS Microbiol. Ecol. 90, 718–730 (2014).
pubmed: 25244497
doi: 10.1111/1574-6941.12430
Darwin, C. & Kebler, L. On the Origin of Species by Means of Natural Selection, or The Preservation of Favoured Races in the Struggle for Life (J Murray, 1859).
doi: 10.5962/bhl.title.82303
van Elsas, J. D. et al. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc. Natl. Acad. Sci. 109, 1159–1164 (2012).
pubmed: 22232669
pmcid: 3268289
doi: 10.1073/pnas.1109326109
De Roy, K. et al. Environmental conditions and community evenness determine the outcome of biological invasion. Nat. Commun. 4, 1383 (2013).
pubmed: 23340423
doi: 10.1038/ncomms2392
Eisenhauer, N., Schulz, W., Scheu, S. & Jousset, A. Niche dimensionality links biodiversity and invasibility of microbial communities. Funct. Ecol. 27, 282–288 (2013).
doi: 10.1111/j.1365-2435.2012.02060.x
Vivant, A.-L., Garmyn, D., Maron, P.-A., Nowak, V. & Piveteau, P. Microbial diversity and structure are drivers of the biological barrier effect against listeria monocytogenes in soil. PLoS One 8, e76991 (2013).
pubmed: 24116193
pmcid: 3792895
doi: 10.1371/journal.pone.0076991
Spor, A. et al. Habitat disturbances modulate the barrier effect of resident soil microbiota on Listeria monocytogenes invasion success. Front. Microbiol. 11, 25 (2020).
doi: 10.3389/fmicb.2020.00927
Gravuer, K. & Scow, K. M. Invader-resident relatedness and soil management history shape patterns of invasion of compost microbial populations into agricultural soils. Appl. Soil Ecol. 158, 103795 (2021).
doi: 10.1016/j.apsoil.2020.103795
Mawarda, P. C., Le Roux, X., Dirk van Elsas, J. & Salles, J. F. Deliberate introduction of invisible invaders: A critical appraisal of the impact of microbial inoculants on soil microbial communities. Soil Biol. Biochem. 148, 107874 (2020).
doi: 10.1016/j.soilbio.2020.107874
Vuolo, F., Novello, G., Bona, E., Gorrasi, S. & Gamalero, E. Impact of plant-beneficial bacterial inocula on the resident bacteriome: Current knowledge and future perspectives. Microorganisms 10, 2462 (2022).
pubmed: 36557714
pmcid: 9781654
doi: 10.3390/microorganisms10122462
Di Salvo, L. P., Cellucci, G. C., Carlino, M. E. & García de Salamone, I. E. Plant growth-promoting rhizobacteria inoculation and nitrogen fertilization increase maize (Zea mays L.) grain yield and modified rhizosphere microbial communities. Appl. Soil Ecol. 126, 113–120 (2018).
doi: 10.1016/j.apsoil.2018.02.010
Ke, X. et al. Effect of inoculation with nitrogen-fixing bacterium Pseudomonas stutzeri A1501 on maize plant growth and the microbiome indigenous to the rhizosphere. System. Appl. Microbiol. 42, 248–260 (2019).
doi: 10.1016/j.syapm.2018.10.010
Renoud, S. et al. Effect of inoculation level on the impact of the PGPR Azospirillum lipoferum CRT1 on selected microbial functional groups in the rhizosphere of field maize. Microorganisms 10, 325 (2022).
pubmed: 35208780
pmcid: 8877547
doi: 10.3390/microorganisms10020325
Hart, M. M., Antunes, P. M., Chaudhary, V. B. & Abbott, L. K. Fungal inoculants in the field: Is the reward greater than the risk?. Funct. Ecol. 32, 126–135 (2018).
doi: 10.1111/1365-2435.12976
Jack, C. N., Petipas, R. H., Cheeke, T. E., Rowland, J. L. & Friesen, M. L. Microbial inoculants: Silver bullet or microbial Jurassic park?. Trends Microbiol. 29, 299–308 (2021).
pubmed: 33309525
doi: 10.1016/j.tim.2020.11.006
Mallon, C. A. et al. The impact of failure: Unsuccessful bacterial invasions steer the soil microbial community away from the invader’s niche. ISME J. 12, 728–741 (2018).
pubmed: 29374268
pmcid: 5864238
doi: 10.1038/s41396-017-0003-y
Bedolla-Rivera, H. I., Negrete-Rodríguez, M. L. X., Gámez-Vázquez, F. P., Álvarez-Bernal, D. & Conde-Barajas, E. Analyzing the impact of intensive agriculture on soil quality: A systematic review and global meta-analysis of quality indexes. Agronomy 13, 2166 (2023).
doi: 10.3390/agronomy13082166
Raaijmakers, J. M. & Weller, D. M. Exploiting genotypic diversity of 2,4-diacetylphloroglucinol-producing Pseudomonas spp.: Characterization of superior root-colonizing P. fluorescens strain Q8r1–96. Appl. Environ. Microbiol. 67, 2545–2554 (2001).
pubmed: 11375162
pmcid: 92906
doi: 10.1128/AEM.67.6.2545-2554.2001
Howie, W. J. Effects of soil matric potential and cell motility on wheat root colonization by fluorescent pseudomonads suppressive to take-all. Phytopathology 77, 286 (1987).
doi: 10.1094/Phyto-77-286
Buddrus-Schiemann, K., Schmid, M., Schreiner, K., Welzl, G. & Hartmann, A. Root colonization by Pseudomonas sp. DSMZ 13134 and impact on the indigenous rhizosphere bacterial community of barley. Microb. Ecol. 60, 381–393 (2010).
pubmed: 20644925
doi: 10.1007/s00248-010-9720-8
Elsas, J. D., Dijkstra, A. F., Govaert, J. M. & Veen, J. A. Survival of Pseudomonas fluorescens and Bacillus subtilis introduced into two soils of different texture in field microplots. FEMS Microbiol. Lett. 38, 151–160 (1986).
doi: 10.1111/j.1574-6968.1986.tb01724.x
Mallon, C. A. et al. Resource pulses can alleviate the biodiversity–invasion relationship in soil microbial communities. Ecology 96, 915–926 (2015).
pubmed: 26230013
doi: 10.1890/14-1001.1
Araujo, M. A. V., Mendonça-Hagler, L. C., Hagler, A. N. & van Elsas, J. D. Survival of genetically modified Pseudomonas fluorescens introduced into subtropical soil microcosms. FEMS Microbiol. Ecol. 13, 205–216 (1994).
doi: 10.1111/j.1574-6941.1994.tb00067.x
Mawarda, P. C., Mallon, C. A., Le Roux, X., van Elsas, J. D. & Salles, J. F. Interactions between Bacterial inoculants and native soil bacterial community: The case of spore-forming Bacillus spp.. FEMS Microbiol. Ecol. 98, 127 (2022).
doi: 10.1093/femsec/fiac127
Taylor, S. C. et al. The ultimate qPCR experiment: Producing publication quality, reproducible data the first time. Trends Biotechnol. 37, 761–774 (2019).
pubmed: 30654913
doi: 10.1016/j.tibtech.2018.12.002
Waiblinger, H.-U., Graf, N., Broll, H., Grohmann, L. & Pietsch, K. Evaluation of real-time PCR results at the limit of detection. J. Verbr. Lebensm. 6, 411–417 (2011).
doi: 10.1007/s00003-011-0669-4
Forootan, A. et al. Methods to determine limit of detection and limit of quantification in quantitative real-time PCR (qPCR). Biomol. Detect. Quantif. 12, 1–6 (2017).
pubmed: 28702366
pmcid: 5496743
doi: 10.1016/j.bdq.2017.04.001
Nutz, S., Döll, K. & Karlovsky, P. Determination of the LOQ in real-time PCR by receiver operating characteristic curve analysis: Application to qPCR assays for Fusarium verticillioides and F. proliferatum. Anal. Bioanal. Chem. 401, 717–726 (2011).
pubmed: 21603916
pmcid: 3132422
doi: 10.1007/s00216-011-5089-x
Berninger, T., González López, Ó., Bejarano, A., Preininger, C. & Sessitsch, A. Maintenance and assessment of cell viability in formulation of non-sporulating bacterial inoculants. Microbial Biotechnol. 11, 277–301 (2018).
doi: 10.1111/1751-7915.12880
Nerek, E., Sokołowska, B., Nerek, E. & Sokołowska, B. Pseudomonas spp. in biological plant protection and growth promotion. AIMSES 9, 493–504 (2022).
doi: 10.3934/environsci.2022029
Ketola, T., Saarinen, K. & Lindström, L. Propagule pressure increase and phylogenetic diversity decrease community’s susceptibility to invasion. BMC Ecol. 17, 15 (2017).
pubmed: 28399832
pmcid: 5387184
doi: 10.1186/s12898-017-0126-z
Jones, M. L., Ramoneda, J., Rivett, D. W. & Bell, T. Biotic resistance shapes the influence of propagule pressure on invasion success in bacterial communities. Ecology 98, 1743–1749 (2017).
pubmed: 28397255
doi: 10.1002/ecy.1852
Wittmann, M. J., Metzler, D., Gabriel, W. & Jeschke, J. M. Decomposing propagule pressure: The effects of propagule size and propagule frequency on invasion success. Oikos 123, 441–450 (2014).
doi: 10.1111/j.1600-0706.2013.01025.x
Amor, D. R., Ratzke, C. & Gore, J. Transient invaders can induce shifts between alternative stable states of microbial communities. Sci. Adv. 6, eaay8676 (2020).
pubmed: 32128414
pmcid: 7030923
doi: 10.1126/sciadv.aay8676
Jiménez, J. A., Novinscak, A. & Filion, M. Inoculation with the plant-growth-promoting rhizobacterium Pseudomonas fluorescens LBUM677 impacts the rhizosphere microbiome of three oilseed crops. Front. Microbiol. 11, 25 (2020).
doi: 10.3389/fmicb.2020.569366
Albright, M. B. N., Sevanto, S., Gallegos-Graves, L. V. & Dunbar, J. Biotic interactions are more important than propagule pressure in microbial community invasions. mBio 11, 02089–20 (2020).
doi: 10.1128/mBio.02089-20
Cornell, C. et al. Do bioinoculants affect resident microbial communities? A meta-analysis. Front. Agron. 3, 25 (2021).
doi: 10.3389/fagro.2021.753474
Wang, Z. et al. Succession of the resident soil microbial community in response to periodic inoculations. Appl. Environ. Microbiol. 87, e00046-e121 (2021).
pubmed: 33637572
pmcid: 8091015
doi: 10.1128/AEM.00046-21
Cipriano, M. A. P. et al. Lettuce and rhizosphere microbiome responses to growth promoting Pseudomonas species under field conditions. FEMS Microbiol. Ecol. 92, fiw197 (2016).
pubmed: 27660605
doi: 10.1093/femsec/fiw197
Roquigny, R. et al. Deciphering the rhizosphere and geocaulosphere microbiomes of potato following inoculation with the biocontrol agent Pseudomonas fluorescens strain LBUM223. Phytobiomes J. 2, 92–99 (2018).
doi: 10.1094/PBIOMES-03-18-0013-R
Cahill, J. F., Kembel, S. W., Lamb, E. G. & Keddy, P. A. Does phylogenetic relatedness influence the strength of competition among vascular plants?. Perspect. Plant Ecol. Evol. Syst. 10, 41–50 (2008).
doi: 10.1016/j.ppees.2007.10.001
Traveset, A. & Richardson, D. M. Plant invasions: The role of biotic interactions—an overview. Plant Invas. Role Biotic Interact. 20, 1–25. https://doi.org/10.1079/9781789242171.0001 (2020).
doi: 10.1079/9781789242171.0001
Mar Vázquez, M., César, S., Azcón, R. & Barea, J. M. Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Appl. Soil Ecol. 15, 261–272 (2000).
doi: 10.1016/S0929-1393(00)00075-5
Nassal, D. et al. Effects of phosphorus-mobilizing bacteria on tomato growth and soil microbial activity. Plant Soil 427, 17–37 (2018).
doi: 10.1007/s11104-017-3528-y
Wu, F. et al. Acinetobacter calcoaceticus CSY-P13 mitigates stress of ferulic and p-hydroxybenzoic acids in cucumber by affecting antioxidant enzyme activity and soil bacterial community. Front. Microbiol. 9, 25 (2018).
doi: 10.3389/fmicb.2018.01262
Sierocinski, P., Soria Pascual, J., Padfield, D., Salter, M. & Buckling, A. The impact of propagule pressure on whole community invasions in biomethane-producing communities. iScience 24, 102659 (2021).
pubmed: 34151242
pmcid: 8192723
doi: 10.1016/j.isci.2021.102659
Muyzer, G., de Waal, E. C. & Uitterlinden, A. G. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59, 695–700 (1993).
pubmed: 7683183
pmcid: 202176
doi: 10.1128/aem.59.3.695-700.1993
Bru, D. et al. Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale. ISME J. 5, 532–542 (2011).
pubmed: 20703315
doi: 10.1038/ismej.2010.130
Berry, D., Ben Mahfoudh, K., Wagner, M. & Loy, A. Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. Appl. Environ. Microbiol. 77, 7846–7849 (2011).
pubmed: 21890669
pmcid: 3209180
doi: 10.1128/AEM.05220-11
Zhang, J., Kobert, K., Flouri, T. & Stamatakis, A. PEAR: A fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30, 614–620 (2014).
pubmed: 24142950
doi: 10.1093/bioinformatics/btt593
Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).
pubmed: 20383131
pmcid: 3156573
doi: 10.1038/nmeth.f.303
Rognes, T., Flouri, T., Nichols, B., Quince, C. & Mahé, F. VSEARCH: A versatile open source tool for metagenomics. PeerJ 4, e2584 (2016).
pubmed: 27781170
pmcid: 5075697
doi: 10.7717/peerj.2584
Quast, C. et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013).
pubmed: 23193283
doi: 10.1093/nar/gks1219
Nawrocki, E. P. & Eddy, S. R. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29, 2933–2935 (2013).
pubmed: 24008419
pmcid: 3810854
doi: 10.1093/bioinformatics/btt509
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
pubmed: 2231712
doi: 10.1016/S0022-2836(05)80360-2
Lozupone, C., Lladser, M. E., Knights, D., Stombaugh, J. & Knight, R. UniFrac: An effective distance metric for microbial community comparison. ISME J. 5, 169–172 (2011).
pubmed: 20827291
doi: 10.1038/ismej.2010.133
Anderson, J. M. & Ingram, J. Tropical Soil Biology and Fertility: A Hand Book of Methods, XF2006286592 (1989).
Dixon, P. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927–930 (2003).
doi: 10.1111/j.1654-1103.2003.tb02228.x
Huet, S. et al. Experimental community coalescence sheds light on microbial interactions in soil and restores impaired functions. Microbiome 11, 42 (2023).
pubmed: 36871037
pmcid: 9985222
doi: 10.1186/s40168-023-01480-7