Importance of Lactic Acid Bacteria as an Emerging Group of Plant Growth-Promoting Rhizobacteria in Sustainable Agroecosystems
, Sabrina Strafella, Pasquale Filannino, Fabio Minervini and Carmine Crecchio *Round 1
Reviewer 1 Report
Comments and Suggestions for AuthorsI find the submitted manuscript interesting and well prepared. Congratulations to the Authors.
There are only a few suggestions that I have.
First, I do not understand the term "plant ecosystem(s)" (in the title and in line 63). Ecology defines an ecosystem as the complex of living organisms, their physical environment, and all their interrelationships in a particular unit of space. So, besides plants, it also includes other organisms. Therefore, I suggest that the title should be changed to: “…in Sustainable Ecosystem (or Agroecosystem) Productivity” or “…in Sustainable Plant Productivity in the Ecosystem (or Agroecosystem)”. I also suggest changing "plant ecosystems" to "agroecosystems" in line 63. However, should you wish to keep the term “plant ecosystem(s)”, you will need to define it, as it is not self-explaining.
My other suggestions are simply technical:
– - it would be more logical to place section 2.4. Bioprotection before section 2.3. Soil bioremediation;
– - in Table 1, it would be reasonable to add horizontal lines to make it easier to distinguish which mode of action is appropriate for which PGPR strain;
– - the sentences "The beneficial outcomes of the application of LAB as biofertilizers and biocontrol agents in several plant species have been summarized in Table 2. A scheme of the biofertilization, bioprotection and biodegradation potential of LAB is 273 shown in Figure 1”. (lines 271-274), as well as Table 2 and Figure 1 should be placed at the end of Chapter 3;
– - the title of Table 2 can be simplified to: “Beneficial effects of lactic acid bacteria in agroecosystem”.
I hope my suggestions will help Authors improve the article in terms of content and form.
Author Response
Dear Reviewer
The authors would like to thank you for your precious time and valuable comments. We have carefully addressed all the comments. The corresponding changes and refinements made in the revised version are summarized in our response below.
Reviewer comments:
There are only a few suggestions that I have.
First, I do not understand the term "plant ecosystem(s)" (in the title and in line 63). Ecology defines an ecosystem as the complex of living organisms, their physical environment, and all their interrelationships in a particular unit of space. So, besides plants, it also includes other organisms. Therefore, I suggest that the title should be changed to: “…in Sustainable Ecosystem (or Agroecosystem) Productivity” or “…in Sustainable Plant Productivity in the Ecosystem (or Agroecosystem)”. I also suggest changing "plant ecosystems" to "agroecosystems" in line 63. However, should you wish to keep the term “plant ecosystem(s)”, you will need to define it, as it is not self-explaining.
Response: Thanks for the note. The reviewer is right and we are sorry for the mistake. We have changed it to “in Sustainable Agroecosystem”.
My other suggestions are simply technical:
– It would be more logical to place section 2.4. Bioprotection before section 2.3. Soil bioremediation;
Response: Thanks for the suggestion. We moved them based on the suggestion and re-arranged the number of references.
– in Table 1, it would be reasonable to add horizontal lines to make it easier to distinguish which mode of action is appropriate for which PGPR strain;
Response: Thanks for the suggestion. In fact, almost all the strains mentioned in each column have common capabilities and it is not possible to separate them in this way.
– The sentences "The beneficial outcomes of the application of LAB as biofertilizers and biocontrol agents in several plant species have been summarized in Table 2. A scheme of the biofertilization, bioprotection and biodegradation potential of LAB is 273 shown in Figure 1”. (lines 271-274), as well as Table 2 and Figure 1 should be placed at the end of Chapter 3;
Response: In fact, the placement of tables and figures in the manuscript is based on the journal's policy, which emphasizes that their place should be after the first reference to them in the text of the manuscript. In any case, this change can be done at the discretion of the editorial office.
– The title of Table 2 can be simplified to: “Beneficial effects of lactic acid bacteria in agroecosystem”.
Response: Thanks for the suggestion. We have edited it accordingly.
Reviewer 2 Report
Comments and Suggestions for AuthorsThe article titled "Importance of Lactic Acid Bacteria as an Emerging Group of PGPR in Sustainable Plant Ecosystem Productivity" presents a comprehensive review on the role of lactic acid bacteria (LAB) in sustainable agriculture as plant growth-promoting rhizobacteria (PGPR). Here are specific comments based on the criteria provided:
The work highlights the potential of LAB as a novel group of PGPR, emphasizing their roles in biofertilization, bioprotection, and enhancing plant growth, which is a valuable addition to the field of sustainable agriculture (lines 27-41).
: The article is structured into sections that logically progress from an introduction of PGPR and the importance of sustainable agriculture to detailed discussions on the functions of LAB in soil and plant health (lines 91-1423).
Each section is detailed, providing specific examples and mechanisms through which LAB contribute to plant growth and stress resistance (lines 777-1256).
The article discusses various mechanisms by which LAB influence plant growth, supported by references to previous research (lines 801-906, 1427-1583).
The conclusions are drawn from reviewed literature and current findings, making them reliable. However, a critical assessment of contradictory or negative impacts of LAB in certain contexts could further strengthen the paper's objectivity.
The paper includes a broad range of references to previous work, demonstrating a thorough literature review (e.g., lines 147-150, 1661-1884).
It covers key studies in the field, from foundational research to the latest findings on LAB as PGPR, ensuring relevance and context (lines 27-41, 1387-1583).
The paper is written in clear, professional English, suitable for an academic audience. Some minor grammatical or typographical errors may require correction to enhance readability (e.g., line 1681-1684 might benefit from grammatical review).
Additional Comments
Figures and Tables: The inclusion of figures and tables (e.g., Table 2, Figure 1) is commendable for illustrating points and summarizing findings (lines 1661-1884). Ensure that these are clearly presented and accurately referenced in the text.
Overall, the paper is a significant contribution to the field, well-organized, scientifically sound, with adequate references, and generally uses correct English. Minor revisions could further enhance its clarity and impact.
Comments on the Quality of English LanguageMinor revisions could further enhance its clarity and impact.
Author Response
Dear Reviewer
The authors would like to thank you for your precious time and valuable comments.
Reviewer comments:
The article titled "Importance of Lactic Acid Bacteria as an Emerging Group of PGPR in Sustainable Plant Ecosystem Productivity" presents a comprehensive review on the role of lactic acid bacteria (LAB) in sustainable agriculture as plant growth-promoting rhizobacteria (PGPR). Here are specific comments based on the criteria provided:
The work highlights the potential of LAB as a novel group of PGPR, emphasizing their roles in biofertilization, bioprotection, and enhancing plant growth, which is a valuable addition to the field of sustainable agriculture (lines 27-41).
The article is structured into sections that logically progress from an introduction of PGPR and the importance of sustainable agriculture to detailed discussions on the functions of LAB in soil and plant health (lines 91-1423).
Each section is detailed, providing specific examples and mechanisms through which LAB contribute to plant growth and stress resistance (lines 777-1256).
The article discusses various mechanisms by which LAB influence plant growth, supported by references to previous research (lines 801-906, 1427-1583).
The conclusions are drawn from reviewed literature and current findings, making them reliable. However, a critical assessment of contradictory or negative impacts of LAB in certain contexts could further strengthen the paper's objectivity.
The paper includes a broad range of references to previous work, demonstrating a thorough literature review (e.g., lines 147-150, 1661-1884).
It covers key studies in the field, from foundational research to the latest findings on LAB as PGPR, ensuring relevance and context (lines 27-41, 1387-1583).
The paper is written in clear, professional English, suitable for an academic audience. Some minor grammatical or typographical errors may require correction to enhance readability (e.g., line 1681-1684 might benefit from grammatical review).
Additional Comments
Figures and Tables: The inclusion of figures and tables (e.g., Table 2, Figure 1) is commendable for illustrating points and summarizing findings (lines 1661-1884). Ensure that these are clearly presented and accurately referenced in the text.
Overall, the paper is a significant contribution to the field, well-organized, scientifically sound, with adequate references, and generally uses correct English. Minor revisions could further enhance its clarity and impact.
Response: Thanks so much for the positive evaluations! We confirm that all presented information within the tables and figure are referenced in the text.
Reviewer 3 Report
Comments and Suggestions for AuthorsDear authors,
Below are the comments from the APPLSCI-2871673 manuscript review. The Manuscript is well written and provides relevant insights into LAB and its potential use as a PGPR.
Detailed comments are in the PDF file.
Comments for author File: 
Comments.pdf
Author Response
Dear Reviewer
The authors would like to thank you for your precious time and valuable comments. We have carefully addressed all the comments. The corresponding changes and refinements made in the revised version are summarized in our response below.
Reviewer comments:
Dear authors,
Below are the comments from the APPLSCI-2871673 manuscript review. The Manuscript is well written and provides relevant insights into LAB and its potential use as a PGPR.
Comment #1 (line 8): Add more details about the benefits of LAB acting as PGPRs.
Response: Thanks for the suggestion. We have added the following statement to the Abstract section:
“In this regard, the ability of LAB to synthesize metabolites including organic acids, phenolic acids and flavonoid derivatives, phytohormones, and antimicrobial substrates is presented.”
Comment #2 (lines 30-34): Provide examples of good agricultural practices that have enabled an increase in production per area (Bradyrhizobium sp. in soybean cultivation in Brazil, Direct planting in the Cerrado Biome of Brazil and revolution in the use of bioinsums also in Brazil, which harvests up to 3 crops per year in the same area).
Response: With respect to the reviewer's opinion, we slightly disagree with this suggestion. In the first paragraph, we tried to briefly mention the challenges that led to the emergence of biological solutions. We believe that dealing with the suggested examples will take us a little away from our goal in the mentioned paragraph.
Comment #3: Add another column highlighting the strain code and commercial product available locally or globally.
Response: Thanks for the comment. We have added the suggested info (e.g. code of strains, GenBank accession number, etc.) from those articles that provided the info to the same column with the name of strains. Please see the green highlighted parts in Tables 1 and 2 in the revised version.
It would be great if we could include complete information for all mentioned strains, but unfortunately, there is not enough information in all articles. Some strains were collected from related microbiology institutes, and there is no information about their commerciality or identification codes in the published articles.
Comment #4: Why hasn't this group received attention like PGPR before? Are there any restrictions on the use of this group of bacteria in agricultural crops used for direct human consumption?
And
Comment #7: Why is this group of bacteria not widely used in agriculture? Are its members cultivable bacteria? What is needed from a biotechnological point of view to disseminate the use of LAB in agriculture as PGPR?
Response: As we mentioned (lines 220-222 in the old version), little attention has been paid to the plant growth-promoting abilities of LAB mainly due to the difficulty of isolating them by plating serial dilutions of rhizospheric soil samples, since enrichment methods using selective culture media have been largely ignored (Chen et al. 2005; Fhoula et al. 2013; Strafella et al. 2021)
Moreover, we discussed in lines 230-232 in the old version, that sometimes the soil conditions prevent the increase of the abundance of LABs and their optimal PGP performance in the soil. For example, a quick breakdown of organic acids in the rhizosphere has been proposed as a limiting factor in the capability of LAB to acidify the rhizosphere to their advantage, thus preventing LAB from being a dominant bacterial group in most agricultural soils (Lamont et al. 2017).
In lines 329-339, we mentioned the need for further work on how to improve the environmental sensitivity of LABs, as a limiting key in their widespread use, and to prolong LABs survival in soils after inoculation mainly in the competition of LAB with indigenous microorganisms. This is important since satisfactory results can be achieved by keeping the LAB bacterial load of the inoculum constant over time. Finally, we suggested future research focusing on the development of efficient microbial formulations that are compatible with routine practices such as seed disinfection and pesticide use, be able to work under different field conditions and soil types, and be safe for humans, animals, and plants.
Chen, YS.; Yanagida, F.; Shinohara, T. Isolation and identification of lactic acid bacteria from soil using an enrichment procedure. Lett appl microbial. 2005, 40, 195–200.
Fhoula, I.; Najjari, A.; Turki, Y.; Jaballah, S.; Boudabous, A.; Ouzari, H. Diversity and antimicrobial properties of lactic acid bacteria isolated from rhizosphere of olive trees and desert truffles of Tunisia. Biomed Res Int. 2013, 2013, 405708.
Lamont, JR.; Wilkins, O.; Bywater-Ekegärd, M.; Smith, DL. From yogurt to yield: Potential applications of lactic acid bacteria in plant production. Soil Biol Biochem 2017, 111, 1-9. https://doi.org/10.1016/j.soilbio.2017.03.015
Strafella, S.; Simpson, D.J.; Yaghoubi Khanghahi, M.; De Angelis, M.; Gänzle, M.; Minervini, F.; Crecchio, C. Comparative Genomics and In Vitro Plant Growth Promotion and Biocontrol Traits of Lactic Acid Bacteria from the Wheat Rhizosphere. Microorganisms 2021, 9, 78. https://doi.org/10.3390/microorganisms9010078
Comment #5: Associate the production of phytohormones with LAB.
and
Comment #6: Associate the biofertilization function with LAB. Cite an example of LAB promoting nutrient cycling and supply to plants.
Response: Thanks for these comments. Actually we have already brought the suggested info and examples in the related sub-section (3.2) and Table 2. In the section referred to by the reviewer, we tried to introduce the PGPR and the importance of sustainable agriculture to link them to further discussions on the functions of LAB in the next sub-sections.
Comment #8: LAB is a well-known group in the food industry. In livestock farming, LAB plays an important role in silage fermentation.
Response: Thanks for the note. We have added silage fermentation to the sentence too.
Comment #9:
Response: This comment is missing in the pdf file.
Comment #10: How does LAB affect soil health and/or quality?
Response: As has been discussed, LABs can improve soil and plant health by regulating soil organic matter and the biochemical cycle, elevating the mineral uptake by plants, secretion of IAA, cytokinin, and siderophore, acetifies the soil, anti-bacterial and anti-fungal activity and detoxify hazardous chemicals (Raman et al. 2022).
Raman, J.; Kim, J.-S.; Choi, K.R.; Eun, H.; Yang, D.; Ko, Y.-J.; Kim, S.-J. Application of Lactic Acid Bacteria (LAB) in Sustainable Agriculture: Advantages and Limitations. Int. J. Mol. Sci. 2022, 23, 7784. https://doi.org/10.3390/ijms23147784
Comment #11: The authors could highlight whether there are commercial LAB-based products on the market.
Response: We have modified Table 2 based on the suggestion. Please see our answer to comment #3 and the green highlighted parts in the modified version of the text.
Comment #12: Improves the resolution of the figure. Adjust the transparency of the background image, this will highlight the other components of the figure.
Response: The reviewer is right about the quality of the figure. We have modified it.
Reviewer 4 Report
Comments and Suggestions for AuthorsReview Comments for Manuscript ID applsci-2871673
The manuscript offers an insightful and comprehensive review of the utilization of plant growth-promoting rhizobacteria (PGPR) and lactic acid bacteria (LAB) as eco-friendly alternatives to synthetic agrochemicals.
The authors have thoroughly examined various aspects of PGPR and LAB, including their functional attributes and mechanisms of action. The discussion on the role of LAB in biological nitrogen fixation, mineral solubilization, biological control of pathogens, and stimulation of phytohormone production is particularly noteworthy. Furthermore, the review provides valuable insights into how these mechanisms contribute to environment-friendly crop productivity and sustainable production systems.
Overall, I believe this manuscript has the potential to make a valuable contribution to the literature on sustainable agriculture. With revisions addressing the aforementioned concerns, I would recommend its publication in Applied Sciences (ISSN 2076-3417).
1- The authors should consider revising the third keyword, as it is repeated in the title. By altering this keyword, it enhances the searchability of the manuscript.
2- In the introduction, it is advisable for the authors to elucidate which Sustainable Development Goal (SDG) the current work aligns with.
3- It would be insightful if the authors delve further into the primary drawbacks associated with the use of agrochemicals, contrasting them with the alternative approaches (such as green agriculture) proposed in this work, thereby highlighting their positive impact.
4- It is recommended that the authors outline all topics to be addressed in the manuscript. Presenting a logical diagram or schema would aid comprehension.
5- Have the authors reviewed prior works based on Life Cycle Analysis regarding the application of sustainable agriculture practices? It would be advisable to emphasize the Life Cycle Analysis to truly assess the effects of replacing synthetic agrochemicals with these sustainable alternative practices. This would enable the identification of areas for improvement or the discovery of new research approaches.
Author Response
Dear Reviewer
The authors would like to thank you for your precious time and valuable comments. We have carefully addressed all the comments. The corresponding changes and refinements made in the revised version are summarized in our response below.
Reviewer #4
Comment #1 The authors should consider revising the third keyword, as it is repeated in the title. By altering this keyword, it enhances the searchability of the manuscript.
Response: Thanks for the suggestion. We have replaced it with “Phyto-stimulation”
Comment #2 In the introduction, it is advisable for the authors to elucidate which Sustainable Development Goal (SDG) the current work aligns with.
Response: Thanks for the note. We have added the following statement in the Introduction section.
“Moreover, the presented sustainable alternatives of agrochemicals receive considerable critical attention in fulfilling part of the United Nations sustainable development goal 15, including on how microbial-based biofertilization can promote sustainable use of agroecosystems and preserve farmlands from degradation.”
Comment #3 It would be insightful if the authors delve further into the primary drawbacks associated with the use of agrochemicals, contrasting them with the alternative approaches (such as green agriculture) proposed in this work, thereby highlighting their positive impact.
And
Comment #5 Have the authors reviewed prior works based on Life Cycle Analysis regarding the application of sustainable agriculture practices? It would be advisable to emphasize the Life Cycle Analysis to truly assess the effects of replacing synthetic agrochemicals with these sustainable alternative practices. This would enable the identification of areas for improvement or the discovery of new research approaches.
Response: We slightly disagree with the reviewer. Although the reviewer is right about adding the disadvantages of using agrochemicals to show the importance of alternatives such as PGPRs, but it should not be overlooked that countless articles in this field have been published in the last few decades and therefore we believe that repeating them in this manuscript may not be interesting for readers.
Also It would be great to involve the topic of agricultural life cycle assessment (LCA) in this manuscript, a suggestion that unfortunately cannot be fulfilled since it has never been in the scope of studies of the authors. Furthermore, we believe that it needs to be discussed in a new manuscript by relevant researchers in this field to comprehensively summarize the impact of agricultural approaches and input-output of the agricultural system on natural resources, human health, and agricultural ecosystem health.
Comment #4 It is recommended that the authors outline all topics to be addressed in the manuscript. Presenting a logical diagram or schema would aid comprehension.
Response: Thanks for the recommendation. We have added Figure 1 accordingly which covers the main topics of the presented manuscript regarding the PGPRs.
