Competition and co-association, but not phosphorous availability, shape the benefits of phosphate-solubilizing root bacteria for maize (Zea mays)

  1. Joseph Williamson
  2. Andrew Charles Matthews
  3. Ben Raymond

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Abstract

Predicting the conditions under which rhizobacteria benefit plant growth remains challenging. Here we tested the hypothesis that benefits from inoculation with phosphate-solubilizing rhizobacteria will depend upon two environmental conditions: phosphate availability and competition between bacteria. We used maize-associated rhizobacteria with varying phosphate solubilization ability in experiments in soil, sterilized soil and gnotobiotic microcosms under conditions of varying orthophosphate availability, while we manipulated the intensity of competition by varying the number of isolates in plant inocula. Growth promotion by microbes did not depend on phosphate availability but was affected by interactions between inoculants: the beneficial effects of one Serratia isolate were only detectable when plants were inoculated with a single strain and the beneficial effects of a competition-sensitive Rhizobium was only detectable in sterilized soil or in microcosms inoculated with single strains. Moreover, microcosm experiments suggested that facilitation of a parasitic isolate, not competitive interactions between bacteria, prevented plants from gaining benefits from a potential mutualist. Competition and facilitation affected colonization of plants in microcosms but growth promotion by Serratia was more affected by inoculation treatment than culturable densities on roots. Experimental manipulation of seed inocula can reveal whether plant growth stimulation is robust with respect to competition, as well as the ecological strategies of different rhizobacteria. From an applied perspective, phosphate solubilization may not provide the mechanism for bacterial growth promotion but may indicate mutualistic potential due to phylogenetic associations. Importantly, benefits to plants are vulnerable to interactions between rhizobacteria and may not persist in mixed inoculations.

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  1. Version published to 10.1099/acmi.0.000543.v3 on Access Microbiology
  3. Version published to 10.1099/acmi.0.000543.v2 on Access Microbiology
  5. Access Microbiology

    Comments to Author

    In this study, the effects of rhizobacterial treatments on plant development, depending on phosphorus availability (soluble and non-soluble P), were examined. The research was carried out under micro-mesocosm and glasshouse conditions using sterile and non-sterile soils. Additionally, competition between the rhizobacterial strains was examined.The results of this study provided new, current, and interesting data to elucidate the relationship between rhizobacterial treatments and plant growth promotion. some comments: line 54-56: - It is normal for this to occur. The authors probably know that PGPR has many different mechanisms, apart from phosphate solubilization. line 61: -Although the introduction explains the hypothesis, aim, and background of the study well, it should be shortened and repetitions should be avoided. line 90-94: - I think that this part is not necessary. line 127-128: -My opinion is an unnecessary detail. The study does not contain any fungal inoculants. line 139-140: -This may not always be possible. Because the inoculated PGPR strains to plant may compete with each other in the rhizosphere and phyllosphere. Indeed, by competition, PGPR may inhibit each other as reported by Xu et al. (2010) "Xu, X., Robinson, J., Jeger, M., & Jeffries, P. (2010). Using combinations of biocontrol agents to control Botrytis cinerea on strawberry leaves under fluctuating temperatures. Biocontrol Science and Technology, 20(4), 359-373." line line 163-164: -In previous studies, have these isolates been checked to see whether they are pathogenic or non-pathogenic on plants? I never seen any data for this. In the result section, I noticed that Rahnella strain W affects tends to adverse plant growth. Could Rahnella strain W be an opportunistic pathogen on plants? and also I have not reached other plant promotion traits of these strains like siderophore production, N2 fixation etc. I think that these traits could be effective as well as phosphate solubilization on plant growth parameters under conditions including insoluble P, and also microbial competition. For example: "Asselin, J. E., Eikemo, H., Perminow, J., Nordskog, B., Brurberg, M. B., & Beer, S. V. (2019). Rahnella spp. are commonly isolated from onion (Allium cepa) bulbs and are weakly pathogenic. Journal of applied microbiology, 127(3), 812-824. https://doi.org/10.1111/jam.14340" line 164: - Due to the selected parameters of isolates, you can provide information in the introduction as to why IAA production was taken into consideration. line 170: -In my opinion, 16S rRNA gene sequence analysis can provide accurate identification at the species level (Clarridge, 2004). Why didn't use a species name? "Clarridge J. E., 3rd (2004). Impact of 16S rRNA gene sequence analysis for identification of bacteria on clinical microbiology and infectious diseases. Clinical microbiology reviews, 17(4), 840-862. https://doi.org/10.1128/CMR.17.4.840-862.2004" line 472- 475: -Which PGPR mechanism could have been effective alternatively in the plant growth promotion of Serratia isolate X? I think you should have given information on other PGPR traits ( for example IAA or siderophor production potential ect.) of isolates of this study. line 494: -Using mixed inocula probably results in interspecific competition among PGPR strains. For instance, although Stenotrophomonas isolate Z is more competitive than other strains in this study, It colonized more effectively plant roots which were not co-inoculated with other strains. line 530-534: -This is a correct determination. However, we cannot call harmful (parasitic) microorganisms PGPR like Rahnella strain W. line 617: - please, check all references and utilize of author's guidelines for this.

    Please rate the manuscript for methodological rigour

    Good

    Please rate the quality of the presentation and structure of the manuscript

    Good

    To what extent are the conclusions supported by the data?

    Strongly support

    Do you have any concerns of possible image manipulation, plagiarism or any other unethical practices?

    No

    Is there a potential financial or other conflict of interest between yourself and the author(s)?

    No

    If this manuscript involves human and/or animal work, have the subjects been treated in an ethical manner and the authors complied with the appropriate guidelines?

    Yes

  6. Access Microbiology

    Comments to Author

    The Present manuscript" Competition and co-association, but not phosphorous availability, shape the benefits of phosphate solubilising root bacteria for maize (Zea mays) is good piece of work, While major revisions are required before the publication can be accepted, this work highlighted beautifully how ecological assessments of rhizobacterial interactions can be done out cheaply and efficiently in high throughput microcosm studies. Major issue/suggestion A] Abstract need to add few experimental data so that reader can take interest to read the manuscript. B] Clear hypothesis is missing in introduction section, so author must add and reframe objective point wise. i- Line 107 to 119 authors reframe the contents and add suitable recent updates, like direct mechanism of PGPR, see Front. Microbiol., 14 July 2022 Sec. Microbial Symbioses Volume 13 - 2022 | https://doi.org/10.3389/fmicb.2022.916488; & mixed mechanism-siderophore Volume 13 - 2022 | https://doi.org/10.3389/fmicb.2022.898979; https://doi.org/10.1016/j.crsust.2021.100063 For exopollysaccharides https://doi.org/10.1080/02648725.2022.2163812, for phosphate Chauhan, P.K., Upadhyay, S.K. Mixed Consortium of Salt-Tolerant Phosphate Solubilizing Bacteria Improves Maize (Zea mays) Plant Growth and Soil Health Under Saline Conditions. Mol Biotechnol (2023). https://doi.org/10.1007/s12033-023-00771-6. ii- Line 144 to 152 In this study, "we identified phosphate-solubilising and phosphate-non-solubilising bacteria that were associated with our study host Zea mays [36, 37]. These strains were from genera previously described as PGPRs: Rahnella [40]; Rhizobium [41]; Stenotrophomonas [42] and Serratia [43] and were used to inoculate Zea mays seeds in a greenhouse mesocosm experiment and controlled microcosm experiments. We hypothesised that P- solubilising bacteria could promote plant growth more effectively in orthophosphate- deficient, insoluble-P-rich condition when compared to conditions with non-limiting orthophosphate. We also hypothesized that microbial competition could limit the benefits derived from inoculation with PGPRs." This statement look like as part of results, justify? please reframe these lines, and avoid to use unnecessary hypothesis at several places in the introduction section, Flow of language is missing in entire manuscript, please improve or take advise from expert. C] Material & Method section i-Line 164 Zea-associated This may be Zea root -associated ii- Seeds were sterilised in aliquots of 100 using bleach and ethanol as described previously [37]. What is 100? Write details about seed sterilization technique see SEED STERLIZATION of Zea https://doi.org/10.1016/j.envres.2022.113081. iii- Why authors collect data /harvest only one time Z. mays plants were left to grow for 28-29 days., author must be collect data after 60 or 90 DAS, please justify? The way of data collection shows the less fitness of experiment. D] Discussion section need to completely reframe, read to hard while results presented by authors are good. E] Authors should add separate section of Conclusion and future perspective including significance of present findings

    Please rate the manuscript for methodological rigour

    Satisfactory

    Please rate the quality of the presentation and structure of the manuscript

    Poor

    To what extent are the conclusions supported by the data?

    Partially support

    Do you have any concerns of possible image manipulation, plagiarism or any other unethical practices?

    No

    Is there a potential financial or other conflict of interest between yourself and the author(s)?

    No

    If this manuscript involves human and/or animal work, have the subjects been treated in an ethical manner and the authors complied with the appropriate guidelines?

    No: Plant microbe

  7. Access Microbiology

    Comments to Author

    In this manuscript Williamson and co-authors analyzed promotion of Zea mays growth by phosphate solubilizing and non-solubilizing [maize] root derived rhizobacteria. The article is written in comprehensible language, is well structured, and conclusions correspond to the results obtained. 1. Methodological rigour, reproducibility and availability of underlying data Authors previously described in detail PGPR, in this article their comprehensive analysis is carried out 2. Presentation of results 3. How the style and organization of the paper communicates and represents key findings Methods & Results are described in detail, the illustrative material (Figures, plots) well complements the text of the manuscript. 4. Literature analysis or discussion Paper contains a detailed analysis of the literature in the sections Introduction and Discussion. 5. Any other relevant comments The manuscript can be accepted in its current state.

    Please rate the manuscript for methodological rigour

    Very good

    Please rate the quality of the presentation and structure of the manuscript

    Very good

    To what extent are the conclusions supported by the data?

    Strongly support

    Do you have any concerns of possible image manipulation, plagiarism or any other unethical practices?

    No

    Is there a potential financial or other conflict of interest between yourself and the author(s)?

    No

    If this manuscript involves human and/or animal work, have the subjects been treated in an ethical manner and the authors complied with the appropriate guidelines?

    Yes

  8. Version published to 10.1099/acmi.0.000543.v1 on Access Microbiology