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Agricultural Enzymes, Phosphatases, Peptidases, and Sulfatases and the Expectations for Sustainable Agriculture
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Ronivaldo Rodrigues da Silva* Instituto de Biociências, Letras e Ciências Exatas, Universidade Estadual Paulista Júlio de Mesquita Filho (UNESP), São José do Rio Preto, São Paulo 15054-000, Brazil carbon (C), nitrogen (N), sulfur (S), and phosphorus (P). A set of physical, chemical, and biological factors contribute to soil health,1 and in this context, enzymes play an important role in maintaining soil fertility. Among the enzymes mentioned in this work, it is important to highlight the phosphatases. These enzymes are essential for maintaining the phosphorus content of the soil; this is a critical component of adenosine triphosphate (ATP) and nucleic acids within cells. Phosphorus is a limiting element in soil and can be assimilated by cells only in the soluble inorganic form.1,2 Sulfatases are also important enzymes responsible for mineralizing organic sulfate, making it available for uptake by microorganisms and plants. Peptidases, in turn, are enzymes that hydrolyze peptide bonds in proteins and peptides. These enzymes are fundamental for the recycling of carbon and provide a source of nitrogen that is accessible to soil organisms.3,4 On the basis of the demand for sustainable technologies, the INTRODUCTION use of such enzymes has emerged in agricultural sciences. The The rising demand for food to meet the increasing population world market for enzymes for agricultural use has led to a profit has necessitated the intensive use of pesticides and fertilizers in of USD 246.9 million in 2016, with a trend that indicates a agriculture. This improves planting and harvesting but entails a progressive increase in future years (https://www. high cost on the environment. Among other environmental grandviewresearch.com/industry-analysis/agriculturalconsequences, the use of pesticides has caused the death of enzymes-market). The use of peptidases to provide peptide bees, directly influencing the pollination of many plants, the hydrolysates for stimulating plant growth has displayed great contamination of soil and rivers, and consequent harm to potential as a substitute for chemical fertilizers.3,4 Collagenases humans and other animals. and keratinases have been used to obtain agricultural peptide In view of these disadvantages, sustainable agriculture has hydrolysates from animal viscera and chicken feathers, become increasingly prominent in recent years. Reducing the respectively.4 use of chemical fertilizers and pesticides is one of the main The advances achieved in this sector have already expectations for an agricultural system capable of producing demonstrated the broad market for biocatalysts. Companies more organic products through ecologically safe means. that stand out in the production of enzymes and the The importance of microbial activity in soil has long been development of microbial solutions for agricultural purposes recognized. At the end of the 19th century, the famous Russian include Novozymes, Creative Enzyme, Enzyme India Pvt. Ltd., scientist, Sergei N. Winogradsky, in his pioneering work, was Afrizymes, and Elemental Enzymes. A summary of some of already demonstrating the importance of bacteria in recycling these enzymes and their role in agriculture is presented in sulfur and nitrogen. Since then, soil microbiology has been a focus of research. In the present day, enzyme technology offers Table 1. an alternative method for reducing the use of certain The advantage of applying enzymes to the soil is that they agricultural chemicals. Here, we will focus on agricultural mineralize organic matter, making nutrients accessible for enzymes, in particular phosphatases, peptidases, and sulfatases. absorption by plants, without polluting the soil, rivers, and air. Furthermore, in the case of peptidases, the organic matter used for the preparation of peptide hydrolysates can be derived from WHY ARE ENZYMES IMPORTANT TOOLS FOR residues of industrial activity, such as animal viscera and SUSTAINABLE AGRICULTURE? chicken feathers. Even if the use of these enzymes does not The soil naturally harbors an arsenal of enzymes derived from allow for the total replacement of chemical fertilizers in the plants (roots and residues), soil animals, and microorganisms (living and dead). The enzymes can be cell-associated or free. These enzymes play an important role in the decomposition of Received: March 21, 2019 organic matter, promoting the recycling of nutrients, such as
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© XXXX American Chemical Society
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DOI: 10.1021/acs.jafc.9b01784 J. Agric. Food Chem. XXXX, XXX, XXX−XXX
Viewpoint
Journal of Agricultural and Food Chemistry Table 1. Enzyme Application in Agriculture method of catalysis
role in agriculture
phosphatase
enzyme
hydrolase
enzyme class
hydrolysis of ester bonds involving a phosphate group in organic material
sulfatase
hydrolase
peptidase
hydrolase
hydrolysis of ester bonds involving a sulfate group in organic material hydrolysis of peptide bonds in proteins and peptides
cellulase
hydrolase
hydrolysis of β-1,4 glycosidic linkages within cellulose
amylase xylanase
hydrolase hydrolase
hydrolysis of α-1,4 glycosidic linkages within starch hydrolysis of β-1,4 glycosidic linkages within xylan
β-glucosidase
hydrolase
urease
hydrolase
hydrolysis of β-1,4 glycosidic linkages within short dextran chains, such as cellobiose, cellotriose, and cellotetraose hydrolysis of urea fertilizer, releasing NH3 and CO2
release of phosphate, making it soluble and accessible for plant uptake, maintenance of the soil phosphorus content releasing sulfate accessible for soil organisms, sulfur cycling releasing amino acids accessible for soil organisms, cycling of carbon and nitrogen decomposition of plant biomass: plant cell wall degradation decomposition of plant biomass (starch) decomposition of plant biomass: plant cell wall degradation providing monosaccharides to heterotrophic soil organisms
dehydrogenase
oxidoreductase
oxidation of organic compounds; activity of this enzyme in the soil is related to the microbial community
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near future, the decreasing use of these harmful compounds already denotes a great advance. In addition to improving the availability of nutrients in the soil, there are promising reports of using peptidases in postharvest fruits for delaying the development of pathogenic fungi. The peptidase from the yeast Aureobasidium pullulans has shown promising results in reducing the growth of the pathogenic fungi Botrytis cinerea and Monilinia fructicola in apple.5 This idea of improving the biopreservation of food using enzymes is a gateway to the study of maximizing the storage time of fresh vegetables. In this discussion, particular attention has been paid to some of the enzymes involved in biogeochemical cycles (C, N, S, and P); however, the agricultural enzyme market also includes enzymes such as β-glucosidase, cellulase, xylanase, urease, and dehydrogenase1 (Table 1).
2 1 3 and 4 1 1 1 1 1 1
REFERENCES
(1) Rao, M. A.; Scelza, R.; Gianfreda, L. Soil enzymes. In Enzymes in Agricultural Sciences; Gianfreda, L., Rao, M. A., Eds.; OMICS Group eBooks: Foster City, CA, 2014; pp 10−43. (2) Margalef, O.; Sardans, J.; Fernández-Martínez, M.; MolownyHoras, R.; Janssens, I. A.; Ciais, P.; Goll, D.; Richter, A.; Obersteiner, M.; Asensio, D.; Peñuelas, J. Global patterns of phosphatase activity in natural soils. Sci. Rep. 2017, 7, 1337. (3) Silva, R. R. Keratinases as an alternative method designed to solve keratin disposal on the environment: Its relevance on agricultural and environmental chemistry. J. Agric. Food Chem. 2018, 66, 7219−7221. (4) Silva, R. R. Enzymatic synthesis of protein hydrolysates from animal proteins: Exploring microbial peptidases. Front Microbiol 2018, 9, 735. (5) Banani, H.; Spadaro, D.; Zhang, D.; Matic, S.; Garibaldi, A.; Gullino, M. L. Biocontrol activity of an alkaline serine protease from Aureobasidium pullulans expressed in Pichia pastoris against four postharvest pathogens on apple. Int. J. Food Microbiol. 2014, 182− 183, 1−8.
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FUTURE DIRECTIONS In this viewpoint, I have proposed evidence for the contribution of enzymes to agriculture. The importance of reducing the use of agricultural chemicals to animal and environmental health is not a new concept. A worldwide movement to reduce the toxicity of agricultural chemicals has driven demand for the implementation of enzymes in the soil. This viewpoint offers brief insight into agricultural enzymes and their market value. Continuous investigation will be required to implement these enzyme technologies in crop fields and minimize the risks associated with contamination from agricultural practices. This will help to ensure that the growing demand for food can be met without compromising the quality of the water, soil, and air. Enzyme technology has already been playing a role in providing alternatives to agricultural chemical application to improve soil health.
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making nitrogen available for assimilation by plants after urea fertilization of the soil sensitive bioindicator relating to soil fertility
reference
AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. ORCID
Ronivaldo Rodrigues da Silva: 0000-0002-6504-8406 Notes
The author declares no competing financial interest. B
DOI: 10.1021/acs.jafc.9b01784 J. Agric. Food Chem. XXXX, XXX, XXX−XXX
