Integrating Ecological Principles for Addressing Plant Production Security and Move beyond the Dichotomy ‘Good or Bad’ for Nitrogen Inputs Choice

Round 1

Reviewer 1 Report

Dear Authors

In the manuscript presented for review "Stories behind the history of nitrogen as a Gospel of choice" , the authors present many well-known facts from the past that are nothing new for the scientific community. The reader has the impression that the considerations are popular science, not scientific, more of philosophical sciences, not agronomic sciences. I suggest supporting many of the cited facts with figures that would make the authors' message more credible, e.g.

- the amount of nitrogen introduced into soil in the form of mineral, natural and organic fertilizers (even estimated data) over the years, globally and locally (world, continents, regions, countries);

- the degree of nitrogen accumulation and loss in these areas (leaching, volatilization of gaseous forms, runoff in river basins, amounts delivered to seas and oceans);

- yields of plants and amounts of nitrogen aborted with them;

- amounts of nitrogen biologically reduced in symbiotic systems and by free-living microorganisms;

- nitrogen deposit in dry and wet rainfall;

- return to soil of nitrogen contained in municipal waste.

The authors have actually suggested two main ways of solving the presented problems of feeding humanity and at the same time protecting agroecosystems: work on the genotype of plants, and increasing the role of bio-fertilizers combined with reducing the application of mineral fertilizers. However, many questions arise: will genetic engineering not become a threat if the manipulations are too widely used? When we notice negative effects similar to the effects of excessive application of synthetic fertilizers or plant protection products. Or maybe the right way is to obtain nitrogen self-nutrition of all plant species, similar to legume plants, which naturally use the huge amount of nitrogen N2 in the atmosphere? More broadly, is mankind in need of research aimed at improving the existing state, or rather a breakthrough discovery that will guarantee us access to a large amount of safe food (after all, the light bulb was not invented by improving the candle)?

Author Response

In the manuscript presented for review “Stories behind the history of nitrogen as a Gospel of choice”, the authors present many well-known facts from the past that are nothing new for the scientific community. The reader has the impression that the considerations are popular science, not scientific, more of philosophical sciences, not agronomic sciences. I suggest supporting many of the cited facts with figures that would make the authors’ message more credible, e.g.

• the amount of nitrogen introduced into soil in the form of mineral, natural and organic fertilizers (even estimated data) over the years, globally and locally (world, continents, regions, countries);

- the degree of nitrogen accumulation and loss in these areas (leaching, volatilization of gaseous forms, runoff in river basins, amounts delivered to seas and oceans);

- yields of plants and amounts of nitrogen aborted with them;

- amounts of nitrogen biologically reduced in symbiotic systems and by free-living microorganisms;

- nitrogen deposit in dry and wet rainfall;

• return to soil of nitrogen contained in municipal waste.

Authors: We agree with the Reviewer and to clarify the aim of our manuscript we clearly stated in the introduction that this is a revision work of a whole group, started in 1985. Being a revision, it builds on consolidated knowledge and presents the main marks in a critical way. 

Nevertheless, we understand the Reviewer’s point and added some important numbers based on the different groups such as Galloway, Erismann and Schlesinger.

“Since N is required for plants photosynthesis (e.g., chlorophyll, enzymes) [26,27], crop productivity relies heavily on N fertilisation. From 1972 to 2022 world population has increased by more than 100%, rising agricultural demand to feed people. N fertilizer consumption by the Haber-Bosch process increased from 82 Tg N yr to 110 Tg N yr (34%) [28]. Cultivation-induced biological nitrogen fixation (C-BNF) has also increased in several agricultural systems, with crop, pasture, and fodder legumes being the most important. The C-BNF estimate for 1970 was 11.5 Tg N and, because of the increase in soybean and meat production over the past five decades, increased to more than 40 Tg N in 2020 [29]. The large fertilizer consumption enlarged cereal and meat production in 20% and 26%, respectively, but increased reactive nitrogen (Nr) creation by 120% [30]. N availability to plants depends on the amount present in the soil and on the rate at which N cycling occurs through the soil-plant system. However, when soil N availability increases (e.g., upon fertilizer application, peak in N mineralization), N is easily lost from the root soil profiles of eco- and agro-ecosystems by runoff, leaching, denitrification, volatilization and crop harvesting.

On a global scale, creation and use are identical, as there are no internal transfers. This makes Nr creation a good indicator of global Human reactive N production. The loss of Nr in the environment increased from approximately 15 Tg N in 1860 to 226 Tg N in 2020 [29]. In this century, the increase in consumption of fertilizer N by Haber-Bosch process was due to two drivers, East and South Asia development [28]. Although, there is a substantial variation by region, process and time, Haber-Bosch process is the most important source of new Nr creation in all regions. The exception is Latin America where the majority of Nr creation is C-BNF, mainly due to the large-scale soy production [29].

The authors have actually suggested two main ways of solving the presented problems of feeding humanity and at the same time protecting agroecosystems: work on the genotype of plants, and increasing the role of bio-fertilizers combined with reducing the application of mineral fertilizers. However, many questions arise: will genetic engineering not become a threat if the manipulations are too widely used? When we notice negative effects similar to the effects of excessive application of synthetic fertilizers or plant protection products. Or maybe the right way is to obtain nitrogen self-nutrition of all plant species, similar to legume plants, which naturally use the huge amount of nitrogen N2 in the atmosphere? More broadly, is mankind in need of research aimed at improving the existing state, or rather a breakthrough discovery that will guarantee us access to a large amount of safe food (after all, the light bulb was not invented by improving the candle)?

Authors: We partly agree with the Reviewer because we focused on plant nutrition and soil ecology and not in genetic engineering. We decided to exclude any study on genetic engineering projects aiming at better plant performance (in terms of production and plant nutrient assimilation). Further, when we mention the importance of plant genotype, we are considering the traditional methods and not just genetic engineering. Actually, when the Reviewer suggests obtaining self-nutrition for all crops, this would require genetic engineering, which is not our approach or suggestion. By contrast, we intend to show the importance of an ecological approach when we are dealing with all dilemmas we still have to maintaining food production with minimum environmental impacts.

Reviewer 2 Report

The paper provides a very good overview over the importance of nitrogen (N) in agricultural systems and the history about research on N use in agriculture. While the historic story until the 20 th centrury is well presented, the paper suggests a new era with biofertilizers in the 21st century. The description about biofertilizers is rather ideologically than scientifically driven and cannot be published in a scientific journal. 

This judgment is further based on the fact that the authors do not define "biofertilizers" or provide a solid reference, which explains the concept behind biofertilizers. While this reviewer totally agrees with the problem statement of modern agriculture, no proof is presented for a better agriculture, with the proposed sustainable agriculture.

To this reviewer it is not clear, how a concept as the "one health" approach can help to address challenges of nitrogen management. 

Specific remark: no valid reference is given to the "Law of the maximium". This reviewer does not see this law as accepted by the scientific community, even though it is plausible to some extent.

Author Response

The paper provides a very good overview over the importance of nitrogen (N) in agricultural systems and the history about research on N use in agriculture. While the historic story until the 20th century is well presented, the paper suggests a new era with biofertilizers in the 21st century. The description about biofertilizers is rather ideologically than scientifically driven and cannot be published in a scientific journal. 

This judgment is further based on the fact that the authors do not define "biofertilizers" or provide a solid reference, which explains the concept behind biofertilizers. While this reviewer totally agrees with the problem statement of modern agriculture, no proof is presented for a better agriculture, with the proposed sustainable agriculture.

Authors: We agree with the Reviewer. We are sorry that within our revision this definition was not clear. We added this text to contribute for a better clarification:

“In response to the global issue of misuse and overuse of pesticides and mineral fertilizers, feeding the increased global population is further challenged by limited availability of agriculture land. Thus, the requirement today is to have a production system which has a higher productivity in a small area and time for cultivation. Besides plant, microbial biotechnology can potentially help in developing sustainable agriculture practices, since microbes play a vital role in determining the fertility and soil structure and in reducing problems associated with the use of chemicals fertilizers [1]. The development of alternate, sustainable and cost-effective biologically available nutrient resources can be achieved with microbial inoculants, acting as biofertilizers. The term “biofertilizer” describes soil live microorganisms that increase plant growth and development acting through various mechanisms: nutrient uptake, minimizing nutrient loss, excretion of phytohormones, controlling plant pathogens [2] protecting plants from different biotic and abiotic stress and pollutants detoxification [3]. More and more, biofertilizers gained relevance in agricultural industries and are viewed as key components of sustainable agriculture. As a result, the global biofertilizer market reached a value of 2.3 billion US dollars in 2020 and it is projected to increase to almost double in 2026 (https://www.marketsandmarkets.com/Market-Reports/compound-biofertilizers-customized-fertilizers-market-856.html)."

No proof is presented for a better agriculture

Authors: We agree with the Reviewer and therefore clarified with the following additions

“Although the use of microorganisms in agriculture is not new [4], the complexity of functions and interactions in plant-associated microbiomes as well as its performance and persistence in the environment is yet to be harnessed [5]. Microbial inoculants can be considered safe, low-cost, and convenient additives that are a nature-based option for promoting plant growth and quality, and disease control [6,7]. Researchers play an important role in the transfer of technology to farmers but studies to understand the needs and preferences of target consumers are also needed. Therefore, research into widespread use of biofertilizers is one of the mainstream in scientific work towards the sustainability of agriculture, minimizing environmental hazards and soil nutrient losses (Fig. 2). In view of the above stated facts, the long-term use of biofertilizers arises to be productive and accessible to marginal and small farmers because it would be the viable option to increase productivity per unit area, while reducing environmental impacts and external N inputs. To help the function of whole systems, agricultural area are not cleared out facilitating the attraction of different pollinators or pest deterrents. This does not mean that there are no constraints. On the contrary, there are still technological, financial and environmental constraints before it can be widespread. But the understanding of the whole ecological web and connectivity is the pillar and a new paradigm that even European Union is interested to follow, according to its Green Deal and The Farm to Fork strategy.”

To this reviewer it is not clear, how a concept as the “one health” approach can help to address challenges of nitrogen management. 

Authors: We agree with the Reviewer, and this was clarified with the following:

“To employ the “One Health” concept, which predicted the integration of the interface with ecosystems in the “One Medicine” concept, we need an approach that is holistic and transdisciplinary and incorporates ecological expertise in applying the ecosystem approach. It is now more knowledgeable that the sustainability of agro-ecosystems depends on their ability to deliver multiple ecosystem services, rather than food and feed production alone. In an anthropocentric point of view, “healthy” soils, plants and animals in an agro-ecosystem is seen in the services they provide to humankind. From an ecological point of view, values and qualities of all organisms within an ecosystem, independently of their utility to human societies, are recognized. Being this a revision within an agronomic perspective the “One Health” concept is here focused on plant productivity, though with an ecological and holistic perspective. This implies that to follow a “One Health” concept we need to focus in a smaller impact on the agricultural soil environment, and a smaller dependence on nutrient inputs. Thus, we need to identify the thresholds beyond which irreversible changes might occur, to understand if they follow the unravelling trajectories of native ecosystems and their symbiotic interactions. Particularly, when we are facing climate change and biotic invasions of disease vectors may ruin crop quality. Therefore, the challenge is to identify those thresholds for soil functioning, since it degradation causes the disappearance of key microbe species and larger dependence of external inputs for plant production.”

Specific remark: no valid reference is given to the “Law of the maximium”. This reviewer does not see this law as accepted by the scientific community, even though it is plausible to some extent.

Authors: we agree with the Reviewer and therefore added the following:

“Following von Liebig’s law of the minimum, production grows linearly until the fertilizer reaches a critical dose till the time at which another factor (whether a mineral or not) becomes limiting to growth. It was Mitscherlich (1912) who, after years of experimentation, stated the Law of Diminishing Returns to express the decreasing marginal productivity outputs as levels of the limiting factor are raised. These observations led Voisin (1903-1964), to the formulation of two new fertilizer laws in (1960s) known as the Law of the Maximum and Law of the priority of biological quality. His concern was for the risk of considering only yield and ignore soil conservation and the "biological quality" of the collected product. He tried to establish the importance on the relationship between crop production and fertilizer levels to achieve productive crops as crucial knowledge for the monitoring of fertility programmes, the development of corrective strategies for the soil as well as for the economic use of resources. According with Liebig’s and Mitscherlich laws returns from fertilization are proportional to the difference between maximum and current productions, in such a way that the returns tend to zero as production approaches its maximum value [8]. Thus, the Law of the Maximum says that “an excessive amount of nutrient availability in soil limits the effectiveness of other substances and in consequence leads to decreased yields”.

Reviewer 3 Report

Dear Authors

               The manuscript " Stories behind the history of nitrogen as a Gospel of choice " is quite carefully written, and deals with a very interesting theme efficiency of nitrogen. It is very important theme because in near future we will bi forced to apply new (innovate) methods to produce sufficient amount of food. Nitrogen/fertilization (production and application) along with other important factors will play major role in battle with food insecurity and malnutrition.

Introduction is well written, but it will be good to add some information about climate change and how it will affect on nitrogen efficiency and global food production.

In part 2. Plant nutrition: The history of humans on Earth in my opinion it is important to mention the Mitscherlich's Law of Diminishing Returns and new breakthrough in science when we taking about Haber-Bosch process for example: Solid solution for catalytic ammonia synthesis from nitrogen and hydrogen gases at 50 °C and Electrifying the Haber–Bosch.

Some minor comments:  

1.       Line 26. First sentence needs reference

2.       Figure 1. Right part of the branch – maybe 20^th century needs to be in the bottom

3.       Line 189 – 190 – I think that the driving force in 20^th century was not only chemical progress but also genetics (see green revolution)

4.       Line 288 Tray to better explain the controversy surrounding ammonium transport systems and mechanisms (it is very interesting part and I think that the readers would like to know more about this topic)

                                                                                                                                       Sincerely yours,

                                                                                                                            Reviewer

Author Response

The manuscript " Stories behind the history of nitrogen as a Gospel of choice " is quite carefully written, and deals with a very interesting theme efficiency of nitrogen. It is very important theme because in near future we will be forced to apply new (innovate) methods to produce sufficient amount of food. Nitrogen/fertilization (production and application) along with other important factors will play major role in battle with food insecurity and malnutrition.

Introduction is well written, but it will be good to add some information about climate change and how it will affect on nitrogen efficiency and global food production.

Authors: We thank this remark and included some related sentences: 

Increase of temperature may produce positive impacts on agriculture in northern countries, while in southern countries water shortage may cause lower harvested yields. This means that climate change may affect differently NUE of crops which are critical for addressing the present challenges of food security and environmental degradation. Here we discuss the fundamental advances in the technological advances in fertilizer use, plant-microbe interactions and plant nutrition towards better agricultural practices with less negative impacts on the environment and human health.

In part 2. Plant nutrition: The history of humans on Earth in my opinion it is important to mention the Mitscherlich’s Law of Diminishing Returns and new breakthrough in science when we taking about Haber-Bosch process for example: Solid solution for catalytic ammonia synthesis from nitrogen and hydrogen gases at 50 °C and Electrifying the Haber–Bosch.

Authors: We agree and thanks the remark of the Reviewer. We included the following: 

“Following von Liebig’s law of the minimum, production grows linearly until the fertilizer reaches a critical dose till the time at which another factor (whether a mineral or not) becomes limiting to growth. It was Mitscherlich (1912) who, after years of experimentation, stated the Law of Diminishing Returns to express the decreasing marginal productivity outputs as levels of the limiting factor are raised. These observations led Voisin (1903-1964), to the formulation of two new fertilizer laws in (1960s) known as the Law of the Maximum and Law of the priority of biological quality. His concern was for the risk of considering only yield and ignore soil conservation and the "biological quality" of the collected product. He tried to establish the importance on the relationship between crop production and fertilizer levels to achieve productive crops as crucial knowledge for the monitoring of fertility programmes, the development of corrective strategies for the soil as well as for the economic use of resources. According with Liebig’s and Mitscherlich laws returns from fertilization are proportional to the difference between maximum and current productions, in such a way that the returns tend to zero as production approaches its maximum value [8]. Thus, the Law of the Maximum says that “an excessive amount of nutrient availability in soil limits the effectiveness of other substances and in consequence leads to decreased yields”. These laws, next to the Liebig’s law of the minimum, are the basis of the present-day systems of fertilization diagnostics in agriculture.”

Some minor comments:  

1.       Line 26. First sentence needs reference

Authors: We agree with the Reviewer and added a reference 

2.       Figure 1. Right part of the branch – maybe 20th century needs to be in the bottom.

Authors: We don’t know if the Reviewer understood the graph evolution. The figure was arranged to be read in a clockwise direction, so, the sense was to start from the left and finish in century 21st in the bottom right.

3.       Line 189 – 190 – I think that the driving force in 20th century was not only chemical progress but also genetics (see green revolution) 

Authors: We agree with the Reviewer included the following:

While the driving force in agriculture in the 20^th century was the widely understood chemical progress (the dominant part of which were mineral fertilizers) and the generation of an explosion of knowledge and technology towards the development of  genetically engineering crops [9], with its boom and sophistication in the 21st century. Taking advantage of being in a metabolomics and transcriptomics era, today's challenge is to merge and integrate all knowledge: from classical crop breeding to crop engineering and from laboratories to replicated field trials.

4.       Line 288 Try to better explain the controversy surrounding ammonium transport systems and mechanisms (it is very interesting part and I think that the readers would like to know more about this topic).

Authors: We agree with the Reviewer and added the following:

Much of ammonium sensitiveness of plants where explained by the mainly occurrence of NH₃ diffusion across biological membranes, independently of the strong evidence that a high affinity NH₄⁺ transport system is over a broad range of organisms. Apparently, transport of ammonium across cellular membranes is conserved throughout all domains of life and the NH₄⁺ deprotonation process may be a mechanistic feature conferring selectivity against K⁺ and for NH₃ transport after NH₄⁺ recruitment.