Soil Health and Sustainable Agriculture

updates Abstract: A healthy soil acts as a dynamic living system that delivers multiple ecosystem services, such as sustaining water quality and plant productivity, controlling soil nutrient recycling decomposition, and removing greenhouse gases from the atmosphere. Soil health is closely associated with sustainable agriculture, because soil microorganism diversity and activity are the main components of soil health. Agricultural sustainability is defined as the ability of a crop production system to continuously produce food without environmental degradation. Arbuscular mycorrhizal fungi (AMF), cyanobacteria, and beneficial nematodes enhance water use efficiency and nutrient availability to plants, phytohormones production, soil nutrient cycling, and plant resistance to environmental stresses. Farming practices have shown that organic farming and tillage improve soil health by increasing the abundance, diversity, and activity of microorganisms. Conservation tillage can potentially increase grower's profitability by reducing inputs and labor costs as compared to conventional tillage while organic farming might add extra management costs due to high labor demands for weeding and pest control, and for fertilizer inputs (particularly N-based), which typically have less consistent uniformity and stability than synthetic fertilizers. This review will discuss the external factors controlling the abundance of rhizosphere microbiota and the impact of crop management practices on soil health and their role in sustainable crop


Introduction
Soil health has been defined by Doran and Zeiss [1] as "the capacity of a soil to function as a vital living system within ecosystem and land use boundaries to sustain plant and animal production, maintain or enhance water and air quality, and promote plant and animal health." Soil health is an intrinsic characteristic of a soil. It is recognized as a list of characteristics that define its health and place it taxonomically. Soil quality, conversely, is an extrinsic characteristic of soils and changes with the desired use of that soil by humans. It may relate to agricultural output and capacity to support wildlife, to protect watershed, or provide recreational outputs.
The rapid projected increase in world population to 8.9 billion people by 2050 will lead to higher demands for agricultural products [2]. High food demands and the shortage of new agricultural land development in the future will require doubling crop yields using sustainable means. Scientists can make a substantial contribution to global sustainability of the agricultural lands by translating scientific knowledge on soil function into practical methodologies that enrich grower's knowledge to evaluate the sustainability of their management practices. Two sustainable agricultural management strategies are targeted to increase soil organic matter and reduce erosion through improvements in plant matter, and respond quickly to any changes occurring in the soil ecosystem, acting as accurate indicators for specific functions in the soil environment [21]. Microbial community functions and their relation with the soil and plant can establish a sustainable soil ecological environment for supporting crop growth, development, and long term yields. Therefore, an understanding of microbial communities' functions, behavior and communication processes in soil and plants are critical for prevention of unexpected management practices before onset of non-repairable damage in the agroecosystem. In fact, understanding microbial activities will provides consistent diagnostics of sustainable soil health and crops production [9].
Soil biota represents one of the largest reservoirs of biodiversity on earth [22]. Global distribution of soil biodiversity ( Figure 1) and soil functions are critical for advancing global sustainability because it incorporates essential components including the habitat for aboveground and underwater biota, climatic factors, water quality, pollution remediation, and food production [23,24]. Soil biota affects ecosystem stability by regulating plant diversity, aboveground net primary production, and species asynchrony [22]. (1) The distribution of microbial soil carbon developed by Serna-Chavez and colleagues [25). This dataset was used as a proxy for soil microbial diversity. (2) The distribution of the main groups of soil macrofauna (used as a proxy for soil fauna diversity). "Global Soil Biodiversity Maps" associated to the Global Soil Biodiversity Atlas, developed by the European Soil Data Centre (ESDAC), Joint Research Centre of the European Commission, June 2016 [26]. Permission to reprint this map was obtained from the ESDAC.

Soil Biodiversity Index
Root-associated soil biota promotes ecosystem stability by influencing how plant species response to changes in the environment; for example by improving plant adaptation to extreme stresses (drought, salinity, and temperatures) induced by climate changes [22]. However, recent reports postulated that global soil biodiversity is threatened (Figure 2), especially in areas with high human populations and intensive land use practices [23]. Soil biodiversity stressors included intensive human use, climate change, and loss of aboveground biodiversity, overgrazing, soil organic matter decline, pollution, soil erosion, and land degradation [26]. Therefore, identifying the threats and intervention to soil biodiversity is critical for global agricultural sustainability. and global agricultural monitoring systems (ground truth data), and consequently to the sustainable development of our agricultural systems.
Healthy soil was shown to suppress pathogens, sustain biological activities, decompose organic matter, inactivate toxic materials and recycle nutrient, energy, and water [31]. Karlen et al. [32] defined soil quality as "the capacity of specific kind of soil to function, within natural or managed ecosystem boundaries, to sustain plant and animal productivity, maintain or enhance water and air quality, and support human health and habitation." Further, a broader defining view to soil quality was provided by Bouma et al. [33] as "the intrinsic capacity of a soil to contribute to ecosystem services, including biomass production." The concept of soil quality allows practical applications with regards to targeted ecosystem services [34]. Soil quality is an increasingly popular concept that encompasses soil biological characteristics and functions in close interaction with chemical and physical properties [35]. As previously indicated, the terms "soil quality" and "soil health" are used as synonymous in the literature. However, they may be differentiated in terms of timescale; "soil health" indicates condition of soil in a short period and "soil quality" over a longer period, much analogous to the condition of a human at a particular time (health) and long time period (quality of life) [36]. Soil health and soil quality terms were used as measurements of soil status, and their assessment is aimed to monitor the influence of present, past, and the future of land use on agricultural sustainability [37].
Unsuitable agricultural practices such as soil salinization, acidification, compaction, crusting, nutrient deficiency, reduction in soil biota biodiversity and biomass, water imbalance, and disruption of elemental cycling reduce soil quality [38]. Normally, soil biota are associated with the suppression of pathogenic organisms, nutrient cycling and detoxification of water storage and responds rapidly to soil management practices [1,39]. There are strong relationships between soil biota, soil fertility, and plant health [40]. The role of soil biota in the improvement of land productivity and soil fertility through biological processes was recognized as a key strategy towards agricultural sustainability [41].

Distribution of Soil Microorganisms
Soil aggregates provide the physical environment for microorganisms and play key roles in determining the total number of microorganisms [42]. In humic rendzina (heavy loam calcareous soil) soil, the number of bacteria, actinomycetes, and fungi located in aggregates from 1-3 mm was higher than in those of aggregates 5-7 mm [42]. In addition, climate, vegetation, total organic carbon, and pH may affect the population density of soil microbes [43]. The assessment of environmental and management factors on the diversity and abundance of rhizosphere microbes showed that soil type was an important variable that affected the microbial population [44]. While clay soil indirectly increased bacterial population through the changes in root length and soil chemical composition (pH, P and K), fungal biomass was linked with the enhanced above-ground plant yield [44].
The rhizosphere surrounds plant root zone and is composed of three zones; soil, the rhizoplane (root surface), and the root itself, which is inhabited by endophytic microorganisms [ 45]. The rhizosphere convers at least 2 mm of the rhizosplane but its effect extends out to 10 mm [46] and in some cases like the vesicular arbuscular mycorrhizae, it extends beyond the depletion zone at the root surface [47]. The rhizosphere is a complex hot spot of microorganisms [48] fungi, bacteria, nematodes, protozoa, algae, archaea, viruses, and arthropods [49]. The diversity of microorganisms is greater close to the rhizoplane, but it decreases at distant rhizoplane zones. This was explained by the carbon concentration, which has a direct correlation with the distance from the rhizoplane [46]. Moreover, the release of root exudates and organic material is essential for active microbiome development, a term called "rhizosphere effect" [SO]. Interestingly, the complex interactions in the rhizosphere showed that all components (roots, soil, and microbes) could be manipulated or engineered to sustain plant growth and development [51]. For example, a better understanding of the rhizosphere root-soil microbe's interactions and their relationships can help to reduce our dependence on chemical fertilizers by using beneficial microbes [52].
Studies on habitat-specific functional microbial communities as prominent indicators raise hope for developing regional or agro-climatic, zone-specific microbial inoculants for successful implications in agriculture and environment [9]. The development and efficiency of commercial microbial inoculants such as AMF, biofertilizers, and microbe-based decomposers offer farmers the potential to reduce synthetic farm inputs (fertilizers and pesticides) and stimulate the opportunity of integrated nutrient and pest management practices for sustainable agriculture [9]. However, when adding exogenous beneficial bacteria into agricultural soils, it is important to analyze the cost-benefit and explore the potential reduction in fertilizer inputs. Current investigations introducing Bacillus spp. into clay soils is under way in a sweet onion production system in Texas (Leskovar et al., unpublished).
Soil and microrhizosphere organisms are considered bio-indicators of soil quality due to their sensitivity and response to small changes in abiotic stresses [50] and their effects on plant structure, composition, and productivity [53]. In fact, it has been postulated that plant productivity under different environmental conditions is correlated with below ground diversity [54]. The rhizosphere microorganisms can promote plant growth and protection from pathogen attack by using a range of mechanisms, such as improving plant nutrient use efficiency, production, selective uptake of Fe and P [15,55] Beneficial rhizosphere microorganisms such as nitrogen-fixing bacteria, mycorrhizal fungi, plant growth promoting rhizobacteria (PGPR), biocontrol microorganisms, mycoparasitic fungi, and protozoa are the most widely studied rhizosphere organisms for their beneficial effects on plants (  Complex mechanisms are involved in plant growth promotion, development, and protection by PGPR, including biofertilization, phytostimulation, and biocontrol [62].

Beneficial nematodes
Biofertilization improves plant nutrient acquisition by providing plants nutrients directly, prompting root growth as well as sustaining beneficial symbiotic relationships [72]. Various microbial taxa have the capacity to access nutrients (P and N) from organic fertilizers and soil residue or to fix atmospheric N, improve water uptake and act as biocontrol agents [73]. The most well-known environmentally friendly biofertilizers for sustainable agriculture are those belonging to Azotobacter, blue green algae, Rhizobium, and Azospirillum

Nematodes
Evidence is growing that the massive diversity of soil biota contributes significantly to shaping above ground biodiversity, the functioning of terrestrial ecosystem, and ecological responses of those ecosystems to current and future environmental change [24]. Recent studies have shown that the diversity of below ground soil biota communities can affect aboveground plant community components (diversity, productivity, abundance, and adaptation to stress factors) and consequently influence ecosystem stability and resilience [22].
Nematode biodiversity in the agroecosystems is associated with the soil ecological condition. Nematodes have been used in studies of sustainability, as biological indicators of soil quality [106]. Soil nematode communities (structural form and function) have the potential to provide an overview of soil processes because most nematodes are active throughout the year and can provide a measure of the biotic and functional status of soils [107]. Nematodes have been recommended as biological indicators for soil quality assessment because they provide a habitat for biodiversity and are involved in nutrient recycling process [108]. However, comparative studies at very large or trans-national level among climatic zones should be carried out with caution because nematode communities differ among bio-geographical zones and land uses within each bio-geographical zone [108].
Worldwide, the estimate yield loss by parasitic nematode is about 12.3% [14]. Plant diseases caused by nematodes are difficult to control because of their hidden nature. Nematodes can form disease complexes with microorganisms and increased crop loss [14]. Conversely, beneficial nematodes help plants feeding on bacteria and fungi and release minerals to soil [109]. Those beneficial nematodes have the ability to respond quickly to soil chemical, physical, and biological changes because they are ubiquitous, have diverse feeding behaviors, and a range of life strategies [109,110]. In addition, free-living beneficial nematodes (Discolaimus, Tripyla and Prionchulus) enhance plant growth through the release of N compounds that are produced as a byproduct of feeding on soil microbes [111].
Nematodes that feed on nematode (bacterivores), as well as algivores and fungivores are useful bio-indicator for soil health [112,113]. Predatory nematodes in the orders Mononchida, Dorylaimida, and Diplogasterida feed on the soil microorganisms and plant parasitic nematodes and release minerals into the soil [114,115]. Omnivorus nematodes such as Pristionchus are capable of both microbial feeding and predatory feeding on other nematodes. A healthy soil has adequate biological diversity and nutrient cycling [116]. Nutrient cycling and availability depends on various soil trophic microorganisms (bacteriovorous, fungivorous, omnivorous, and predatory nematodes) which play a significant role in the mineralization (release) of nutrients from organic matter. Studies have shown predatory nematodes increasing nutrient mineralization and consequently plant productivity in buffalo grass (Bouteloua gracilis) and perennial ryegrass (Lolium perenne) [111,115,117]. Overall, a healthy, well-structured, fertile soil has a massive and wide range of free-living nematodes (specifically, beneficial nematodes) with a good balance between fungal and bacterial feeders as well as having predatory and omnivorous nematodes [118].

Soil Borne Pathogens
Soil-borne pathogens cause significant crop loss worldwide. A healthy soil community has a diverse food web that keeps diseases within the control levels through predation, competition, and parasitism [119]. Soil-borne pathogens, such as Rhizoctonia spp., Verticillium spp., Phytophthora spp., Pythium spp., and Fusarium spp. have negative effects on plants growth causing root rot, seedling damping off, branch dieback, wilting, and blight diseases [120). Soil pathogens can survive for many years in the absence of their target host plant by producing persistent structures, such as sclerotia, microsclerotia, chlamydospores, or Oospores [62). As a result, they are difficult to detect and manage [121). Sustainable agriculture requires healthy soils to help suppress soil pathogens (Table 1) and effective management of soil-borne inhibitors and pathogens. Thus, by knowing what pathogens are present (identification of causal agents) and the spatial distribution, suitable cultural practices (crop rotation, managing crop residues, and resistance cultivars), soil disinfection, and solarization, biological and chemical control strategies can be followed (Table 1). Soil borne pathogens are critical biological components of soil biodiversity and these microorganisms can be managed to improve soil quality and plant health in sustainable agriculture (Table 1) [122). Understanding the role of different soil managements practices (Table 1) is key to enhance the agricultural soil health and contribute to long-term crop productivity [122). Certain crop cultural practices that are designed to manage soil biodiversity in the agroecosystem by suppressing soil borne diseases and improving diversity are shown in Table 1 [123).
systems (e.g., Netherlands where the conventional yield gap was significantly larger), most studied regions had relative yields fairly close to the overall average [150].
Organic farming can improve soil physical and chemical properties. For example, organic systems in a clay soil increased soil water content (-15%) and retention capacity (10%) and reduced soil bulk density (8%) in the top 20 cm soil layer as compared to conventional systems [151). In addition, organic farming is a good source of macro-nutrients (Table 2). For example, in a long-term (18 years) study using chemical and organic fertilization regimes, N storage of organic manure treated soil was significantly higher (50%) in the 20 cm topsoil than conventional chemical fertilizers [136). In another long-term study (21 years) of organic and conventional farming, nutrient input (N, P, K) in the organic soil was 34 to 51% lower than in the conventional, whereas Ca 2 + and Mg 2+ were (30-50%) higher [137).
Short-term, conventional farming normally has a greater capacity to increase yield compared to organic farming [16]. In addition, organic farming is more costly for growers due to the high labor demand for weed and pest control and the lack of uniformity and stability of organic fertilizers [155]. The main challenge in organic farming is to synchronize nutrient release, specifically N, with seasonal growth demand of crops [155). Organic materials do not release adequate amount of N to succeeding crops beyond 6 to 8 weeks after incorporation [155). Low N supply during the crop growth stages leads to a reduction in leaf chlorophyll content, inefficient water use and subsequently lower growth and yield [156,157]. In a recent study in globe artichoke, plants grown following conventional farming had higher growth and yield than those from organic farming [16). That study also showed that soil amendment using organic farming reduced soil NO 3 -, P, K, Mg 2+ and increased Ca 2+ compared to conventional, while significantly improving soil respiration-CO 2 (soil health indicator) by 20-fold compared to conventional. In addition, the organic system increased head quality components, specifically chlorogenic acid by 31 % and cynarin by 12% compared to the conventional system. Similarly, organic soil amendments (organic vs conventional fertilizers) increased marketable yield, ascorbic acid and phenolic compounds in collard (Brassica oleracea) and kale (Brassica oleracea) [158).
Meta-data studies of conventional and organic growing systems showed that organic products (fruits, vegetables, and grains) had lower NO 3 -content and pesticide residue levels and higher nutrient (Fe 3+ , Mg 2+ , P) and vitamin C [159,160].
Although organic farming is less productive than conventional, organic yield can approach the same productivity after cropping for 10-13 years [138). Overall, organic farming is the best system to improve soil and fruit quality, but it may not be the best option for farmers (short-term) when yield is the primary target [16). Therefore, a productivity gap between organic and conventional systems can be a matter of time, and that long-term organic farming may result in higher stability of soil microbial communities and soil processes [138).
Crop rotation with legumes usually provides the most N for organic farming systems. However, providing adequate amount of N to crops in organic culture can be challenging because the nutrient (specifically N) release process is quite slow compared to mineral fertilizers [155). Therefore, growers use plant-and animal-based organic fertilizers to meet the essential crop requirements. However, commercially available organic fertilizers are more costly than chemical fertilizers [156), because they are more difficult to produce and require large biomass (plant-based fertilizers) to guarantee consistently positive plant responses. Therefore, the choice of plant-or animal-based organic fertilizer is critical to sustain crop yield and gain profits in organic farming. Several plant-based (e.g., leguminous crop and maize meals) and animal-based (e.g., blood and fish meals, feathers, bones, and composted-manure) fertilizers are available commercially for organic growers [156,161]. Plant-based fertilizers such as leguminous crops have been used widely as green manures to increase the available N in the soil [162,163]. Legumes can fix atmospheric Nin the soil, reduce the risk ofNo 3 -leaching, improve soil physical and chemical properties as well as fruit quality [162,164]. In artichoke, organic soil amended with alfalfa meal had higher soil respiration (soil health indicator) and head phytochemicals than soil amended with animal-based fertilizers (fish meal, blood meal, and chicken manure) [147). However, artichoke grown in soil amended with animal-based fertilizer (chicken manure) had higher head yield and input cost (N: $US 31 kg-1 for blood meal, $US 28 kg-1 for chicken manure, $US 44 kg-1 for fish meal, and $US 74 kg-1 for alfalfa meal) than those amended using, alfalfa meal [147). Long-term, plant-based fertilizers (leguminous crop and maize meals) can be an ideal choice for improving soil health, while animal-based (blood and fish meals, feathers, bones and composted-manure) may be a superior option for organic growers when yield and cost are the main concerns, especially short-term.

Tillage Practices
Tillage practices affect soil chemical and physical properties, as well as fruit quality and crop yield as reported in watermelon and rice-maize cropping systems [9,165]. Adopting useful tillage practice is a prerequisite to sustain soil health and crop production [166). Conservation tillage practices (no-tillage, reduced, and strip) can increase soil microbial activities, soil moisture, organic matter, aggregate stability, cation exchange capacity and crop yield [9,165,167,168]. Conservation tillage using permanent beds and strip tillage can potentially increase farmer net income (Table 3) and benefit; cost ratio by increased plant water use efficiency and reduced irrigation water and labor use compared to conventional [165,169]. Al-Kaisi et al. [170) also found that tillage intensity significantly reduced soil macro-and micro-aggregate stability. Conservation tillage practices increased soil available P in the topsoil (0-20 cm) by 3.8%, K by 13.6% and soil organic matter by 0.17% compared to conventional [171). Maintaining crop residues on the top soil surface layer (full cover, no till; partial cover, strip tillage) can also reduce soil erosion and increases soil moisture content [172,173].
soil nutrient cycling for better soil health. Organic system increases soil nutrient mineralization, and microorganism abundance and diversity as well as soil physical properties. Interestingly, organic fertilizer source (plant-or animal-based) can potentially affect microorganism abundance and crop yield. While plant-based fertilizer increases soil microbial abundance, animal-based fertilizer has higher crop yield and lower number of microorganisms. However, organic cultural practices are more costly due to high labor cost and lack of uniformity and stability of organic fertilizers. Overall, plant-based farming can be an ideal practice to increase soil and fruit quality, while animal-based fertilizer would be the preferred for organic farmers seeking higher yield at relatively lower input cost of fertilizers. For tillage practices, conservation tillage (no-tillage, reduced, and strip) improve soil health by enhance soil fungi abundance and activity, earthworm diversity, organic matter, aggregate stability, and caution exchange capacity. In fact, conservation tillage such no-till reduced irrigation water applied (12-25%) and increased water use efficiency (16-24%) and total net returns ($49-281) compared to conventional (e.g., mouldboard, harrow followed with cultivator). However, conservation tillage might increase root-feeding nematodes (harmful to plant roots) compared to conventional. Improved assessment of soil health indicators is necessary to further enhance our understanding on how production strategies and environmental factors affect the physical, biological, and chemical stability and d yn amics of the soil-rhizosphere-plant systems and their impact to short or long term sustainability.