Abstract
The sustainable production of tomatoes (Solanum lycopersicum) is important, and this can be achieved by determining the rate of respiration of microbes in the tomato plants' rhizosphere soil. This study aimed at the potential of microbes to utilize carbon substrates embedded in the rhizosphere soil thereby contributing to the healthy nature of the tomato plants. The potential soil physiochemical features and utilization of carbon substrate by soil microorganisms as a result of their respiration to reveal their functions in the ecosystem were evaluated. The soil samples were amassed from the healthy tomato plant rhizosphere, diseased tomatoes, and bulk soil in this study. The physiochemical features and carbon substrate utilization in the bulk soil samples, and rhizosphere samples of powdery diseased, and healthy tomato plants were assessed. The MicroRespTM procedure was used to determine the community-level physiological profiles (CLPP) employing fifteen (15) carbon (C) substrates selected based on their importance to microbial communities embedded in the soil samples. Our results revealed that various physiochemical properties, moisture content, water retention, and C substrates including sugar, amino acid, and carboxylic acid were greater in HR and the substrates were not significantly different (p < 0.05). The study reveals higher soil respiration in HR as a result of the microbial communities inhabiting HR utilizing more of the C-substrates. This investigation contributes to the tomato plant's healthy state as the microbial communities utilized carbon substrate compared to DR after employing the CLPP assays.
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1 Introduction
Crop growth and development are dependent on the nature of the soil employed for planting (Amare and Desta 2021; Lal et al. 2021; Omotayo and Babalola 2021). Over the years, crop production has increased tremendously with much importance in the feeding of humans and animals globally, alongside eradicating hunger (Adedayo et al. 2022a). Various challenges have been observed in the soil as the population of humans and animals increases, thereby causing the soil to lose its fertility. Biodiversity loss and soil degradation result from substantial changes observed in the soil (Hojjati et al. 2021; Qiu et al. 2021). The exudates produced by the plant root are the major constituents controlling the existence of microorganisms dwelling in the rhizosphere soil (Badri et al. 2013; Chaparro et al. 2014; Savarese et al. 2022). Some studies have revealed how beneficial microbial communities were inhabited by natural disease rhizosphere soils (Ge et al. 2021; Noman et al. 2021; Zhao et al. 2021) and found their way into the soil via the root exudates thereby acting against phytopathogens in the soil. The populations of the microbial communities in these disease soils are not as much as in healthy rhizosphere soil which is why the microorganisms living in the healthy rhizosphere (HR) consumed carbon (C) substrates more than the microorganisms in the diseased rhizosphere (DR) (Wang et al. 2019).
Tomato (Solanum lycopersicum L.) is one of the essential fruits around the world consumed by humans because it contains important carotene, lycopene, vitamins, and minerals (Dorais et al. 2008). The cultivation of tomatoes and other crop plants has added more value to the soil used for agricultural purposes. Microbes living in the rhizosphere of tomato crops carry out an important function in soil structure formation, transformation, and decomposition of various organic compounds likewise removal of toxic compounds (Adedayo et al. 2022b; Ling et al. 2022). The microbes colonizing the soil can gather some compounds, alleviate the nutrient assimilation in plants through root hairs, improve plant growth, and improve defense processes and stress tolerance against biotic and abiotic factors (Dukare et al. 2022).
Carbon sequestration and nutrient cycling are major functions obtained in the soil that help maintain the balance of the sustainable ecosystem (Amoo et al. 2021a; Raj and Jhariya 2021; Zhao and Wu 2021). However, the decomposition of wastes, the profile of microbial functionality, and the cycling of nutrients required more knowledge as a result of soil usage for plantations. C cycling is one of the prominent functions carried out by the microbial communities in the ecosystem (Holmberg et al. 2019; Li et al. 2021a). Luo et al. (2022) indicated that the carbon found in the terrestrial biosphere is made of organic carbon. In a functioning ecosystem, the important function of soil organic matter (SOM) is to retain nutrients, stabilize soil structure, and preserve water-holding capacity (Amoo et al. 2021b). SOM decomposition enables the production of nutritive substances required for adequate plant development (Cardenas et al. 2021). Plants are known to be producers in the feeding hierarchy in the ecosystem which makes them special from other ecobiomes. Tomato plants have been reported by Li et al. (2022) to alter the quantity of C assimilated into the soil which may be prone to unfavorable effects on soil carbon in the atmosphere. As a result, the knowledge of soil C response accelerates the ability of microbes embedded in the soil to break down various C sources to acknowledge the specific changes observed in the soil (Amoo et al. 2021b). The high level of C substrate in soils contributes to a significant improvement in the diversity and functions of microbial communities in agricultural ecosystems, thereby enhancing sustainable agriculture (Adedayo et al. 2022a; Kaul et al. 2021). C source carries out functions like nutrient cycling and its availability to crop plants in rhizosphere soil (Kaul et al. 2021). Plants derive benefit from the microbial community activity in the rhizosphere soil when they assimilate C source as a nutrient, enhance microbe phytohormones regulation, inhibit the proliferation of spoilage organisms, and thus enhance plant health (Bogati and Walczak 2022).
The physicochemical features of the soil samples can control the associations between the microbial communities and the plants. The distribution of microbial species in the soil is associated with various soil properties like pH, organic carbon, ions (Mg+, K+, Ca2+), and nitrogen concentration, among others (Li et al. 2021b). The role of the microbiome in the soil is their potential to respire in soil with certain C substrates that differ structurally to produce community-level physiological profiling (CLPP). The procedure of measuring the substrate required by the microbes in the soil is conducted by employing the CLPP assay (Nwachukwu et al. 2021).
Previous studies have reported the effect of the microbial communities and their functional diversity in the root region soil of tomatoes employing 16 s ribosomal RNA (16S rRNA) gene amplicon sequencing (Hu et al. 2020; Li et al. 2014), internal transcribed spacer (ITS) (Li et al. 2014; Wei et al. 2021), and shotgun metagenomic sequencing among others (Adedayo et al. 2022a, b). The results obtained in these previous studies revealed differences in taxonomical (that revealed the existence and abundance of the microbial communities including Actinobacteria, Planctomycetes, Chloroflexi, Cyanobacteria, Proteobacteria, Ntrospirae, Verrucomicrobia, Deinococcus-Thermus) in Supplementary Fig. 1 and functional diversity (Carbohydrates, Cell Division and Cell Cycle, Cofactors, Vitamins, Prosthetic Groups, Pigments, Fatty Acids, Lipids, Dormancy, and Sporulation, Isoprenoids, Miscellaneous, Nucleosides, and Nucleotides, Clustering-based subsystems, Stress Response, Cell Wall and Capsule, Nitrogen Metabolism, Regulation and Cell signaling, Motility and Chemotaxis, Potassium metabolism, and Photosynthesis) in the rhizosphere (Supplementary Fig. 2), but these studies have not reported respiration profile based as a specific function of improving the healthy status of the tomato plant. Although few reports have shown how microbiomes inhabiting soil consume C substrate for catabolic activity (Hamilton et al. 2021; Lu et al. 2016; Wolińska et al. 2020), yet, no distinct differences in the sequestration of carbon were observed by microbial communities in the soils. So, the multifarious dynamic that controls the microbial communities, their impact, and other functions involving C sequestration is not fully understood. Microbial communities revealed their impact on how to utilize C substrates inhabiting the rhizosphere soil of healthy plants, in order to prevent the existence of negative factors as a result of C feedback (Amoo and Babalola 2019; Amoo et al. 2021b).
MicroResp assay has been employed in this study to differentiate between soil samples in a controlled laboratory environment. It helps to determine soil health, quality, and community-level physiological profiles. This assay considers quantifying microbial respiration through C sources to the point where the microbial population assimilated the C substrates (Enagbonma et al. 2021). This technique is employed to determine the entire soil community-level physiological profiles independent of the microbial population multiplication. Its application in various studies has proven its validity in other procedures (Amoo et al. 2021b; Enagbonma et al. 2021). The study however aimed to evaluate the ability of the rhizosphere microorganisms in the soil samples to utilize C substrates and we speculated that the microbes in HR will carry out higher catabolism by utilizing more C substrates compared to DR and BR.
2 Methodology
2.1 Experimental Location and Sampling
This study was investigated at the North-West University farm (Mmabatho, South Africa) (coordinates 25°47′19.1″S, 25°37′05.1″E; 25°47′17.0″S, 25°37′03.2″; 26°019′36.9″S, 26°053′19.0″E, altitude 159 m above sea level). Little rainfall of about 300 to 600 mm is often experienced with thunderstorms annually in the northwest region of South Africa between August and April summer. The region has a degree of hotness and coldness ranges between 20 and 40 °C. The temperature falls drastically during the winter to 5 °C or less and is experienced between the early months of May and July.
The Roma tomato variety (S. lycopersicum cv Roma VF) has been cultivated for more than six years, and soil has been managed with traditional nitrogen, phosphorus, and potassium (NPK) fertilization. The plantation of the tomato commenced in November 2020. From three plots, bulk and rhizosphere soil samples of tomatoes were collected in three replicates for HR, DR, and BR from an open field in March 2021. The portion of the first site was healthy tomatoes. On the second plot was a diseased tomato (powdery mildew) with the following features: yellow spots on the leaves followed by powdery nature on leaves and stems. The third region of the farmland was regarded as the bulk soil with no tomato plantation. The healthy and diseased plots were 40 m distant from each other, and the bulk plot was 50 m distant from the other plots.
The HR and DR were obtained after soil samples were collected from five different healthy and diseased tomato plants which were pooled together to produce a replicate. So, 3 replicates were produced from 15 tomato healthy and diseased plant rhizosphere soils after being pooled together. However, the same procedure was done for bulk soil too. In March 2021, the soil sampling was conducted, before the harvest season. A sterilized soil auger was employed for the collection of the soil samples around the roots of the plants. The soils were dug to a depth of 4–15 cm deep and were packed into sterile polythene sampling bags. The soil adhering to the roots was also jolted and collected into the plastic bag. The soil samples were kept at − 4 °C in cold boxes and conveyed to the cold room where they were kept at − 20 °C.
2.2 Physiochemical Properties of Soil Samples
The physical and chemical concepts of the tomato rhizosphere and bulk soils obtained were evaluated following standard procedures. Using a pH meter, the soil pH was quantified in the ratio of 1:2.5 (soil:water) while the total carbon was measured by the dry combustion procedure (Santi et al. 2006). Nitrogen forms in soils including nitrate and ammonium were confirmed by the potassium chloride (KCl) extraction method as reported by Bremner and Keeney (1966). Following the method of Mebius (1960), organic carbon was measured. Calcium, magnesium, and potassium ions are determined by the electro‐ultrafiltration (EUF) procedure (Di Meo et al. 2003). The sulfur content of the soil samples was determined as explained by Kotkova et al. (2008). Following the method of Tandon et al. (1968), phosphorus was determined from the soil samples by applying an acid-free vanadate-molybdate reagent for spectrophotometry analysis. Soil organic matter was evaluated following the method of Terefe et al. (2008). Soil samples were subjected to high temperatures (100 °C) to reduce organic content in the soil. The temperature controls evapotranspiration, which impacts the water content of the soil, which is attributed degradation of soil organic matter (Davidson et al. 2000).
2.3 Community-Level Physiological Profile
The moisture content of the soil samples was observed to range from 30 to 60% according to the standard MicroResp method as reported by Campbell et al. (2003). For 7 days, the soil samples were incubated at − 20 °C so that the microorganisms in the soil could accumulate after sieving with a 5-mm sieve (Creamer et al. 2016). Some of the soil samples that contained more than 60% moisture content were air-dried in an incubator above 40 °C for 24 h until their moisture content ranged between 30 and 60% as explained in the MicroResp manual (Renault et al. 2013). The method of Benke and Kearfott (1999) was used to detect the moisture content of soil samples after oven-drying them above 100 °C.
- MC:
-
moisture content
- X:
-
the weight of the soil sample before incubation
- R:
-
the weight of the soil sample after incubation
Water retention (WR) also known as water holding capacity is the ability of the soil samples to hold the amount of water when saturated employing a suitable soil handling method to regulate the moisture content of the soil. In this study, the soil samples used were measured (25 g) and added to filter paper in the funnel. Fifty milliliters of distilled water was added (volume of water used) and allowed to stand for 20 min. The filtered water (F) was measured with the aid of a calibrated measuring cylinder, and the water retention capacity was calculated using the standard (OECD) method for soil water retention capacity as explained by Jakob et al. (2012) used in the study.
The standard MicroResp procedure was conducted by measuring 0.4 g of the soil samples with the calibrated weighing balance and adding them into 96 deep well plates. The deep well plates were covered with Parafilm and incubated in a dark cupboard for 3–5 days. After incubation days, 15 carbon sources were employed to assess the physiological activities together with a control well that contained the soil samples and distilled H2O(l). These substrates employed in the study comprised 4 carbohydrates that include (glucose, lactose, galactose, and maltose), and 5 amino acids (glycine, L-cysteine, L-arginine, L-lysine, and methionine), 5 carboxylic acids that comprise (citric acid, D-malic acid, oxalic acid, pantothenic acid, and salicylic acid), alcohol (mannitol), and distilled water. The weight of the salts required for each soil is calculated as shown below:
- W:
-
the weight of soil required
- MC:
-
moisture content
- WS:
-
the weight of the soil in 96 deep well = 0.4
- K:
-
constant = 30
After obtaining the salt required, 25 mL of distilled H20(l) was added to dissolve the different carbon sources. From the solution of the carbon salts obtained, 25 µL of the solution is added into the deep wells containing 0.4 g of soil samples with the aid of a micropipette.
Colorimetric gel detection plates were prepared as follows: 3 g of agar was measured into a 200-mL conical flask, and 100 mL of distilled H2O was added. The solution was shaken to dissolve undissolved agar powder and further heated in an oven for some minutes. Cresol red (18.75 mg), 0.315 g Na(HCO3)2, and 16.7 g KCl were dissolved in 1 L of distilled H2O(l) to prepare an indicator solution. One hundred milliliters of the agar solution prepared was added to 200 mL of indicator prepared in the water bath at 60 °C at a ratio of 1:2. With the aid of an 8-channel micropipette, 25 µl aliquots were dispensed into a 96-well detection plate of 1.2 mL deep. The dispensed aliquots were allowed to solidify, and the detection plates were kept in a desiccator for 2 days before being used in a dark cupboard. The initial reading of the prepared detection plates at 0 h was measured on the MicroResp™ machine at wavelength 570 nm. It was noted that the initial reading should not exceed 5% after measuring the reading result on the Excel sheet package. This procedure was explained according to the MicroResp manual (Renault et al. 2013).
After the initial reading has been checked, the detection plate is assembled with the 96-deep well and incubated at 25 °C for 6 h. MicroResp™ microplate was employed again to check the final reading according to the manufacturer’s guide (AccuReader M965 + , Taipei, Taiwan) after 6 h of incubation at 570 nm to obtain the absorbance figures. The percentage CO2 and CO2 rate were determined according to the equation below as used by Amoo et al. (2021b).
where A = − 0.2265, B = − 1.606, Ai = normalized absorbance data, and D = − 6.771 according to the standard MicroResp manual.
- %CO2:
-
percentage of carbon dioxide (%).
- CO2 rate:
-
carbodioxide rate (μg CO2-cg−1 h−1).
- vol:
-
volume in the well (μL).
- frh wt:
-
fresh weight of soil in the well (g).
- dry wt:
-
% soil sample dry weight.
- t:
-
incubation time.
2.4 Statistical Analyses
The mean value and standard error obtained in the properties of the soil and C substrate were worked out with Univariate analysis of variance (ANOVA). In the 96-well deep-well plate, the soil samples were replicated three times after adding different carbon sources, so that the mean of the three replicates of the samples was obtained and further employed for statistical analysis to confirm the significant differences (p < 0.05). The significance (p < 0.05) was tested employing Duncan’s multiple range test employing IBM SPSS statistics software 27. Canonical correspondence analysis (CCA) on CANOCO 5 (Microcomputer Power, Ithaca, NY) was adopted to compare the CLPPs among the soil sample properties and the ability to utilize the carbon source. Catabolic diversity was determined by investigating microbial functions after the addition of carbon sources (Brolsma et al. 2017; Enagbonma et al. 2021).
3 Result
3.1 Physiochemical Parameter of the Soil Samples
Changes observed in the soil samples are accompanied by physiochemical properties of the soil samples that include moisture content, soil organic matter (SOM), potassium (K), magnesium (Mg), phosphorus (P), nitrate (NO3), and pH that may have certain effects on the soil as the result of carbon sequestration and nutrient cycling (Yin et al. 2014). Physiological profile modifications of the microbes embedded in the used soil samples were determined and presented as observed in Table 1. The depleted potential to utilize C sources can lead to depleted carbon sequestration with certain effects on the advancement of the planet’s temperature change or global warming (Jiang et al. 2017). Various changes occurring in soil properties are usually associated with reduced functions in the soil. The rhizosphere and bulk soil employed in this study’s physiochemical attributes were determined. The soil sample texture was sandy-loam in nature, which made the soils have high porosity and infiltration (Mortazavizadeh et al. 2022). The soil physicochemical analysis reveals that the soil pH, total C, organic carbon, organic matter, potassium ammonium, and soil nitrate were significantly different across the tomato rhizosphere soil samples and bulk soil as observed in Table 1.
3.2 Moisture Content and Water Retention
The result obtained for moisture content and water retention capacity of the soil samples (HR, DR, and BR) showed that HR has the highest moisture content as well as water retention capacity then DR and BR in order of HR > DR > BR. From the employed soil samples (HR, DR, and BR), the initial weight was measured before incubating the soil in the incubator. After incubation, the final weight was measured. The moisture content was obtained in percentage. The volume of distilled water obtained after the filtration method, and the percentage of water retention obtained as observed in Table 2. This study revealed that HR has the highest water retention compared to DR and BR. This shows the ability of HR to absorb water for crop plant consumption to improve the growth of the plants.
The data present the mean ± standard error. “HR” denotes the rhizosphere soil of a healthy tomato plant; “DR” denotes the rhizosphere of the diseased plant; and “BR” is the bulk soil.
3.3 CLPP of Microorganisms—MicroPlate™
This study revealed consistent responses of C cycling in the HR, DR, and BR. Fifteen carbon substrates and distilled water were employed in the study to assess the activity of soil microbiomes in utilizing these substrates (Figs. 1, 2, and 3). The analyses of CLPP were observed from microbial respiration responses to the substrates. The microorganisms in HR were observed to consume the substrate in abundance unlike those in DR and BR. The substrate consumption is significantly higher in HR (p-values > 0.05) in the order HR > DR > BR with the following listed substrates: glucose, lactose, maltose, glycine, methionine, lysine, malic acid, citric acid, cysteine, oxalic acid, and salicylic acid. The substrates observed to be consumed higher in DR are galactose, arginine, and mannitol. However, pantothenic acid and distilled water were observed to be significantly higher in BR as shown in Supplementary Table 1.
3.4 The Soil Properties and Microbial Communities' Potential
CCA, as used in this study, revealed that total N, org C, Mg, K, N-NO3, and P positively correlated with most of the C substrates that include glucose, maltose, lactose, glycine, lysine, methionine, cysteine, malic acid, salicylic acid, citric acid, and oxalic acid (Fig. 4; Table 1). N-NH4, pH, total C, and SO42− negatively correlated with galactose, arginine, mannitol, and distill H2O, while pantothenic acid was abundant in DR and BR sites (Fig. 4; Table 1). The effect properties of the soil on the physiological potential of the microorganisms were unveiled by employing CCA as observed in Fig. 4. The association among various environmental variables was revealed in the plot. CCA axis 1 explained 31.7% of the total variation and 20.1% on axis 2 of the environmental variables and the metabolic attributes of the soil microbes (Table 1; Supplementary Table S2).
4 Discussion
The application of the MicroResp™ assay to quantify community-level profiling of microbial activity in various soil samples has revealed the latent effects on the microbiomes to soil properties (Enagbonma et al. 2021). This present study affirmed the significant changes that take place in community-level physiological profiles (CLPP) of soil samples or the level of utilization of C substrate among HR, DR, and BR that coincides with the study of Venter et al. (2016). Tomato cultivation has a specific influence on soil structure and microbiomes embedded in its rhizosphere soil. In this study, CLPP assays were employed to compare and reveal the process of metabolism of the microbes in tomato plants’ rhizosphere soil, and control soil, otherwise regarded as bulk soil. The basic concept of the CLPP defines the total amount of carbon consumed, revealing the microbial biomass that uses up a particular C source (Creamer et al. 2016). Pradhan et al. (2020) reported that the metabolic activities and functional diversity of microbiomes increase as a result of the huge amount of carbon source the microbiomes utilize.
The pH of the soil contributes immensely to soil microbiomes’ functions at different levels and soil structure (Ali et al. 2019a; Siedt et al. 2021). Narendra et al. (2015) reported how rhizosphere soil samples obtained from growing tomatoes with pH 6.5 biosynthesize an antioxidant peroxidase and polyphenol oxidase (PPO) contributing to the growth of tomato and further preventing early blight disease from attacking the tomato plant. The report coincides with our study with a pH value of 6.72 protecting the HR tomato plantation from powdery mildew diseases. Organic carbon, total carbon, and nitrogen contribute to the healthy status of tomatoes by preventing disease attacks on tomatoes. Islam and Toyota (2004) reported how organic carbon produced by different compost, nitrogen, ammonium nitrogen (NH4+-N), and nitrate-nitrogen (NO3−-N) inhibition of phytopathogen Ralstonia solanacearum on tomatoes which was in line with our study. We likewise reported the effort of essential nutrients P, K, Mg, and SO42− in preventing the invasion of powdery mildew diseases on tomato plants. These elements were greater in HR. Ali et al. (2019b) reported the effectiveness of organic fertilizer composed of Ca, Mg, N, P, and K in preventing disease and insect attacks on a tomato plant and improving environmental tolerance.
Rhizosphere soil respiration is affected by certain properties among which are temperature, moisture content, and pH. Soil respiration is not sensitive to low temperatures (< 5 °C) but sensitive in the high-temperature range (10–20 °C). When the moisture content of the soil samples was maintained at ≤ 60% of the water holding capacity as employed in this study, respiration will be controlled by SOM. However, the carbon substrates supplied likewise control the respiration level when they interact with other soil properties. While plants are photosynthesizing at high temperatures, soil respiration will increase because of carbon responsiveness to temperature changes when provided with enough carbon substrates (Hunt et al. 2002).
The degradation and rate of utilization of carbon substrate were higher in HR, unlike DR and BR. This is because of the health status of the tomato plant to carry out respiration activity, thereby requiring C sources for catabolic activity. Carbon substrates that include cysteine, glucose, lactose, maltose, glycine, methionine, lysine, malic acid, citric acid, oxalic acid, and salicylic acid were greater in HR; galactose, arginine, and mannitol in DR; and pantothenic acid and distilled water in BR. This showed how the microbial communities inhabiting the soil samples degrade the substrates provided in a control laboratory environment. Our report is in line with the report that explained how Aspergillus tubingensis utilized various C substrates, which include glucose, galactose, lactose, and maltose to inhibit Fusarium solani that brings about soft rot diseases affecting the tomato plant (Kriaa et al. 2015). In this study, various amino acid substrates reported were greater in HR and they include glycine, cysteine, methionine, and lysine, supporting the healthy condition of the tomato plant growth while arginine is greater in DR. Our report corresponds with Alfosea-Simón et al. (2020) that reported how various amino acid impart to the development of tomato plant. Carboxylic acid substrates, including malic acid, citric acid, oxalic acid, and salicylic acid, were abundant in HR, while pantothenic acid is abundant in BR.
After the catabolic activity of soil microbiome profiling, significant differences were observed in the soil samples. The results presented in earlier studies revealed that the MicroResp assay is a proportional biological indicator procedure for analyzing the metabolic potential of soil microbiomes with different soil properties and C sources on different soil samples (Bérard et al. 2014).
The activities of microbes improve healthy plantations, limit the respiration rate in soil, and have the potential to break down C sources (Tahat et al. 2020; Wani et al. 2012). So, there is a rise in the involvement of the plantations' influences in sustainable agriculture. Healthy plant crops are well known to possess huge C substrates in their soil ecosystems, and they possess greater carbon sequestration rates (Akinola and Babalola 2021). Crop plants likewise modified the functional potential of soil microbiomes across sites. However, we confirmed that crop plants have limited potential to break down C sources in the soil during their degradation. Such C sources include alcohol, amino acids, carboxylic acids, and sugars of animal, microbial, and plant origins. The healthy tomato plants provide support to soil organisms to break down C source as observed by reducing the mechanisms obtainable in the soils to break down the soil organic matter.
The canonical correspondence analysis (CCA) plot is often used to show the relationship among environmental variables. Ter Braak and Verdonschot (1995) explain how CCA has been applied to various environmental samples that back up our study. CCA is a multivariate method to elucidate the relationships between biological assemblages of C substrates and the physicochemical properties of the soil samples employed in this study. The method is also employed to reveal environmental gradients from ecological data obtained via soil properties. The soil properties’ effect on the physiological potential of the microbial communities was unveiled by employing CCA (Fig. 4). Most of the C substrates were more significant in the HR site. The important function of sugar in the rhizosphere has been revealed to preserve and stimulate activities of microbiomes for quality performance as explained by Gunina and Kuzyakov (2015). The soil properties do not impart to the microbial population growth in the soil as observed in this study. Other C substrates used in building microbial biomass are amino acids and various carboxylic acids (Gunina et al. 2014; McDaniel and Grandy 2016). The low content of nitrogen compounds (N-NH4) and total C available in the soil explains how low amounts of the amino acid and carboxylic acid substrates were required for assimilation by the microbiome in the rhizosphere soils to build microbial population during the respiration process (Högberg and Read 2006; Lipson and Näsholm 2001).
5 Conclusion
Taken together, this is one of the foremost studies to show how soil microbes influence the utilization of C substrates in the rhizosphere soil of diseased and healthy tomato plants. We employed the MicroResp™ assay to quantify the community-level physiological profile of microbial functionality in diseased and healthy tomato rhizosphere soil and the bulk soil. The study revealed that the microbial communities in the healthy rhizosphere site utilized more carbon substrates due to the higher soil respiration in the healthy rhizosphere, as compared to diseased rhizosphere and bulk soil sites. This shows the impact of microbial catabolism during the respiration profiles of microbial communities in rhizosphere soil samples obtained from healthy, diseased rhizosphere, and bulk soil. More research should be conducted on the activity of C substrate enzymes to improve the healthy nature of tomato plants.
Abbreviations
- BR:
-
Bulk soil
- CCA:
-
Canonical correspondence analysis
- CLPP:
-
Community-level physiological profiles
- DR:
-
Diseased tomato plant rhizosphere
- EUF:
-
Electro‐ultrafiltration
- F:
-
Filtered water
- HR:
-
Healthy tomato plant rhizosphere
- MC:
-
Moisture content
- PPO:
-
Polyphenol oxidase
- SOM:
-
Soil organic matter
- WR:
-
Water retention
References
Adedayo AA, Fadiji AE, Babalola OO (2022) The effects of plant health status on the community structure and metabolic pathways of rhizosphere microbial communities associated with Solanum lycopersicum. Horticulturae 8:404. https://doi.org/10.3390/horticulturae8050404
Adedayo AA, Fadiji AE, Babalola OO (2022) Plant health status affects the functional diversity of the rhizosphere microbiome associated with Solanum lycopersicum. Front Sustain Food Syst 6:1–11. https://doi.org/10.3389/fsufs.2022.894312
Akinola SA, Babalola OO (2021) The fungal and archaeal community within plant rhizosphere: a review on their contribution to crop safety. J Plant Nutr 44:600–618. https://doi.org/10.1080/01904167.2020.1845376
Alfosea-Simón M, Simón-Grao S, Zavala-Gonzalez EA, Cámara-Zapata JM, Simón I, Martínez-Nicolás JJ, Lidón V, Rodríguez-Ortega WM, García-Sánchez F (2020) Application of biostimulants containing amino acids to tomatoes could favor sustainable cultivation: implications for tyrosine, lysine, and methionine. Sustainability 12:9729. https://doi.org/10.3390/su12229729
Ali A, Imran Ghani M, Li Y, Ding H, Meng H, Cheng Z (2019a) Hiseq base molecular characterization of soil microbial community, diversity structure, and predictive functional profiling in continuous cucumber planted soil affected by diverse cropping systems in an intensive greenhouse region of northern China. Int J Mol Sci 20:2619. https://doi.org/10.3390/ijms20112619
Ali M, El-Tokhy A, El-Sherbini M, Abdel-Dayem S, Khpalwak W (2019) Response of growth, yield and fruit quality of tomato (Solanum Lycopersicum L.) to different organic fertilizer treatments under two pest control programs against Tuta absoluta in a new valley-Egypt. J Sustain Agric Sci 45:37–57. https://doi.org/10.21608/jsas.2019.9777.1131
Amare G, Desta B (2021) Coloured plastic mulches: impact on soil properties and crop productivity. Chem Biol Technol Agric 8:4. https://doi.org/10.1186/s40538-020-00201-8
Amoo AE, Babalola OO (2019) Impact of land use on bacterial diversity and community structure in temperate pine and indigenous forest soils. Diversity 11:217. https://doi.org/10.3390/d11110217
Amoo AE, Babalola OO, Stewart FJ (2021) Microbial diversity of temperate pine and native forest soils profiled by 16S rRNA gene amplicon sequencing. Microbiol Resour Announc 10:e00298-e221. https://doi.org/10.1128/MRA.00298-21
Amoo AE, Delgado-Baquerizo M, Babalola OO (2021b) Forest plantations reduce soil functioning in terrestrial ecosystems from South Africa. Pedobiologia 89:150757. https://doi.org/10.1016/j.pedobi.2021.150757
Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM (2013) Application of natural blends of phytochemicals derived from the root exudates of arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288:4502–4512. https://doi.org/10.1074/jbc.m112.433300
Benke RR, Kearfott KJ (1999) Soil sample moisture content as a function of time during oven drying for gamma-ray spectroscopic measurements. Nucl Instrum Methods Phys Res A 422:817–819. https://doi.org/10.1016/S0168-9002(98)01004-3
Bérard A, Mazzia C, Sappin-Didier V, Capowiez L, Capowiez Y (2014) Use of the MicroResp™ method to assess pollution-induced community tolerance in the context of metal soil contamination. Ecol Indic 40:27–33. https://doi.org/10.1016/j.ecolind.2013.12.024
Bogati K, Walczak M (2022) The impact of drought stress on soil microbial community, enzyme activities and plants. Agronomy 12:189. https://doi.org/10.3390/agronomy12010189
Bremner J, Keeney D (1966) Determination and isotope-ratio analysis of different forms of nitrogen in soils: 3. Exchangeable ammonium, nitrate, and nitrite by extraction-distillation methods. Soil Sci Soc Am J 30:577–582. https://doi.org/10.2136/sssaj1966.03615995003000050015x
Brolsma KM, Vonk JA, Mommer L, Van Ruijven J, Hoffland E, De Goede RGM (2017) Microbial catabolic diversity in and beyond the rhizosphere of plant species and plant genotypes. Pedobiologia 61:43–49. https://doi.org/10.1016/j.pedobi.2017.01.006
Campbell CD, Chapman SJ, Cameron CM, Davidson MS, Potts JM (2003) A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl Environ Microbiol 69:3593–3599. https://doi.org/10.1128/AEM.69.6.3593-3599.2003
Cardenas J, Santa F, Kaštovská E (2021) The exudation of surplus products links plant functional traits and plant-microbial stoichiometry. Land 10:840. https://doi.org/10.3390/land10080840
Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803. https://doi.org/10.1038/ismej.2013.196
Creamer RE, Stone D, Berry P, Kuiper I (2016) Measuring respiration profiles of soil microbial communities across Europe using MicroResp™ method. Appl Soil Ecol 97:36–43. https://doi.org/10.1016/j.apsoil.2015.08.004
Davidson EA, Trumbore SE, Amundson R (2000) Soil warming and organic carbon content. Nature 408:789–790. https://doi.org/10.1038/35048672
Di MV, Michele A, Paola A, Pietro V (2003) Availability of potassium, calcium, magnesium, and sodium in “bulk” and “rhizosphere” soil of field-grown corn determined by electro-ultrafiltration. J Plant Nutr 26:1149–1168. https://doi.org/10.1081/pln-120020362
Doerr SH, Thomas AD (2000) The role of soil moisture in controlling water repellency: new evidence from forest soils in Portugal. J Hydrol 231–232:134–147. https://doi.org/10.1016/S0022-1694(00)00190-6
Dorais M, Ehret DL, Papadopoulos AP (2008) Tomato (Solanum lycopersicum) health components: from the seed to the consumer. Phytochem Rev 7:231–250. https://doi.org/10.1007/s11101-007-9085-x
Dukare A, Mhatre P, Maheshwari HS, Bagul S, Manjunatha BS, Khade Y, Kamble U (2022) Delineation of mechanistic approaches of rhizosphere microorganisms facilitated plant health and resilience under challenging conditions. 3 Biotech 12:1–33. https://doi.org/10.1007/s13205-022-03115-4
Enagbonma BJ, Amoo AE, Babalola OO (2021) Biopedturbation by termites affects respiration profiles of microbial communities from termite mound soils. J Plant Nutr Soil Sci 21:2115–2123. https://doi.org/10.1007/s42729-021-00507-y
Ge AH, Liang ZH, Xiao JL, Zhang Y, Zeng Q, Xiong C, Han LL, Wang JT, Zhang LM (2021) Microbial assembly and association network in watermelon rhizosphere after soil fumigation for Fusarium wilt control. Agric Ecosyst Environ 312:107336. https://doi.org/10.1016/j.agee.2021.107336
Gunina A, Kuzyakov Y (2015) Sugars in soil and sweets for microorganisms: review of origin, content, composition and fate. Soil Biol Biochem 90:87–100. https://doi.org/10.1016/j.soilbio.2015.07.021
Gunina A, Dippold MA, Glaser B, Kuzyakov Y (2014) Fate of low molecular weight organic substances in an arable soil: from microbial uptake to utilisation and stabilisation. Soil Biol Biochem 77:304–313. https://doi.org/10.1016/j.soilbio.2014.06.029
Hamilton CD, Steidl OR, Macintyre AM, Hendrich CG, Allen C (2021) Ralstonia solanacearum depends on catabolism of myo-inositol, sucrose, and trehalose for virulence in an infection stage–dependent manner. Mol Plant Microbe Interact 34:669–679. https://doi.org/10.1094/mpmi-10-20-0298-r
Högberg P, Read DJ (2006) Towards a more plant physiological perspective on soil ecology. Trends Ecol Evol 21:548–554. https://doi.org/10.1016/j.tree.2006.06.004
Hojjati SM, Darzi A, Asadi H, Tafazoli M (2021) Changes in soil properties and plant biodiversity after 12 years of rehabilitating livestock farms in the Hyrcanian Forests. Agrofor Syst 95:1493–1503. https://doi.org/10.1007/s10457-021-00658-y
Holmberg M, Aalto T, Akujärvi A, Arslan AN, Bergström I, Böttcher K, Lahtinen I, Mäkelä A, Markkanen T, Minunno F, Peltoniemi M, Rankinen K, Vihervaara P, Forsius M (2019) Ecosystem services related to carbon cycling – modeling present and future impacts in boreal forests. Front Plant Sci 10:1–14. https://doi.org/10.3389/fpls.2019.00343
Hu J, Wei Z, Kowalchuk GA, Xu Y, Shen Q, Jousset A (2020) Rhizosphere microbiome functional diversity and pathogen invasion resistance build up during plant development. Environ Microbiol 22:5005–5018. https://doi.org/10.1111/1462-2920.15097
Hunt JE, Kelliher FM, McSeveny TM, Byers JN (2002) Evaporation and carbon dioxide exchange between the atmosphere and a tussock grassland during a summer drought. Agric Meteorol 111:65–82. https://doi.org/10.1016/S0168-1923(02)00006-0
Islam TM, Toyota K (2004) Suppression of bacterial wilt of tomato by Ralstonia solanacearum by incorporation of composts in soil and possible mechanisms. Microbes Environ 19:53–60. https://doi.org/10.1264/jsme2.2004.53
Jakob L, Hartnik T, Henriksen T, Elmquist M, Brändli RC, Hale SE, Cornelissen G (2012) PAH-sequestration capacity of granular and powder activated carbon amendments in soil, and their effects on earthworms and plants. Chemosphere 88:699–705. https://doi.org/10.1016/j.chemosphere.2012.03.080
Jiang CM, Yu WT, Ma Q, Xu YG, Zou H (2017) Alleviating global warming potential by soil carbon sequestration: A multi-level straw incorporation experiment from a maize cropping system in Northeast China. Soil Tillage Res 170:77–84. https://doi.org/10.1016/j.still.2017.03.003
Kaul S, Choudhary M, Gupta S, Dhar MK (2021) Engineering host microbiome for crop improvement and sustainable agriculture. Front Microbiol 12:1–10. https://doi.org/10.3389/fmicb.2021.635917
Kotkova B, Balik J, Cerny J, Kulhánek M, Bazalova M (2008) Crop influence on mobile sulphur content and arylsulphatase activity in the plant rhizosphere. Plant Soil Environ 54:100
Kriaa M, Hammami I, Sahnoun M, Azebou MC, Triki MA, Kammoun R (2015) Biocontrol of tomato plant diseases caused by Fusarium solani using a new isolated Aspergillus tubingensis CTM 507 glucose oxidase. C R Biol 338:666–677. https://doi.org/10.1016/j.crvi.2015.05.007
Lal R, Bouma J, Brevik E, Dawson L, Field DJ, Glaser B, Hatano R, Hartemink AE, Kosaki T, Lascelles B, Monger C, Muggler C, Ndzana GM, Norra S, Pan X, Paradelo R, Reyes-Sánchez LB, Sandén T, Singh BR, Spiegel H, Yanai J, Zhang J (2021) Soils and sustainable development goals of the United Nations: an International Union of Soil Sciences perspective. Geoderma Reg 25:e00398. https://doi.org/10.1016/j.geodrs.2021.e00398
Li JG, Ren GD, Jia ZJ, Dong YH (2014) Composition and activity of rhizosphere microbial communities associated with healthy and diseased greenhouse tomatoes. Plant Soil 380:337–347. https://doi.org/10.1007/s11104-014-2097-6
Li B, Guo L, Wang H, Li Y, Lai H, Wang X, Wei X (2021a) Bio-organic fertilizers manipulate abundance patterns of rhizosphere soil microbial community structure to improve tomato productivity. 19 October 2021, PREPRINT (Version 1) available at Research Square 1–35. https://doi.org/10.21203/rs.3.rs-852188/v1
Li N, Shao T, Zhou Y, Cao Y, Hu H, Sun Q, Long X, Yue Y, Gao X, Rengel Z (2021b) Effects of planting Melia azedarach L. on soil properties and microbial community in saline-alkali soil. Land Degrad Dev 32:2951–2961. https://doi.org/10.1002/ldr.3936
Li Z, Di Gioia F, Paudel B, Zhao X, Hong J, Pisani C, Rosskopf E, Wilson P (2022) Quantifying the effects of anaerobic soil disinfestation and other biological soil management strategies on nitrous oxide emissions from raised bed plasticulture tomato production. J Environ Qual 51:162–180. https://doi.org/10.1002/jeq2.20324
Ling N, Wang T, Kuzyakov Y (2022) Rhizosphere bacteriome structure and functions. Nat Commun 13:836. https://doi.org/10.1038/s41467-022-28448-9
Lipson D, Näsholm T (2001) The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystems. Oecologia 128:305–316. https://doi.org/10.1007/s004420100693
Lu Y, Rao S, Huang F, Cai Y, Wang G, Cai K (2016) Effects of biochar amendment on tomato bacterial wilt resistance and soil microbial amount and activity. Int J Agron 2016:2938282. https://doi.org/10.1155/2016/2938282
Luo X, Bai X, Tan Q, Ran C, Chen H, Xi H, Chen F, Wu L, Li C, Zhang S, Zhong X, Tian S (2022) Particulate organic carbon exports from the terrestrial biosphere controlled by erosion. CATENA 209:105815. https://doi.org/10.1016/j.catena.2021.105815
McDaniel MD, Grandy AS (2016) Soil microbial biomass and function are altered by 12 years of crop rotation. SOIL 2:583–599. https://doi.org/10.5194/soil-2-583-2016
Mebius LJ (1960) A rapid method for the determination of organic carbon in soil. Anal Chim Acta 22:120–124. https://doi.org/10.1016/S0003-2670(00)88254-9
Mortazavizadeh F, Fatahi A, Asefpour VK, Pagliari PH, Cerdà A, Mirzaei M, Zhang X, Adnan Ikram RM (2022) Effects of ash derived from livestock manure and two other treatments on soil moisture content and water infiltration rate. Irrig Drain Syst 71 (4):1024–1033. https://doi.org/10.1002/ird.2713
Narendra BA, Jogaiah S, Ito SI, Kestur NA, Tran LSP (2015) Improvement of growth, fruit weight and early blight disease protection of tomato plants by rhizosphere bacteria is correlated with their beneficial traits and induced biosynthesis of antioxidant peroxidase and polyphenol oxidase. Plant Sci 231:62–73. https://doi.org/10.1016/j.plantsci.2014.11.006
Noman M, Ahmed T, Ijaz U, Shahid M, Azizullah LD, Manzoor I, Song F (2021) Plant–microbiome crosstalk: dawning from composition and assembly of microbial community to improvement of disease resilience in plants. Int J Mol Sci 22:6852. https://doi.org/10.3390/ijms22136852
Nwachukwu BC, Ayangbenro AS, Babalola OO (2021) Comparative study of microbial structure and functional profile of sunflower rhizosphere grown in two fields. BMC Microbiol 21:337. https://doi.org/10.1186/s12866-021-02397-7
Olowe OM, Ayangbenro AS, Akanmu AO, Kutu FR, Odhiambo JJO, Babalola OO (2023) Comparative insights into the microbial diversity and community structure of Striga hermonthica-infested maize rhizosphere. Appl Sci 13:3260. https://doi.org/10.3390/app13053260
Omotayo OP, Babalola OO (2021) Resident rhizosphere microbiome’s ecological dynamics and conservation: towards achieving the envisioned Sustainable Development Goals, a review. Int Soil Water Conserv Res 9:127–142. https://doi.org/10.1016/j.iswcr.2020.08.002
Qiu L, Zhang Q, Zhu H, Reich PB, Banerjee S, van der Heijden MGA, Sadowsky MJ, Ishii S, Jia X, Shao M, Liu B, Jiao H, Li H, Wei X (2021) Erosion reduces soil microbial diversity, network complexity and multifunctionality. ISME J 15:2474–2489. https://doi.org/10.1038/s41396-021-00913-1
Raj A, Jhariya MK (2021) Carbon storage, flux and mitigation potential of tropical Sal mixed deciduous forest ecosystem in Chhattisgarh. India J Environ Manage 293:112829. https://doi.org/10.1016/j.jenvman.2021.112829
Renault P, Ben-Sassi M, Bérard A (2013) Improving the MicroResp™ substrate-induced respiration method by a more complete description of CO2 behavior in closed incubation wells. Geoderma 207–208:82–91. https://doi.org/10.1016/j.geoderma.2013.05.010
Santi C, Certini G, D’Acqui LP (2006) Direct determination of organic carbon by dry combustion in soils with carbonates. Commun Soil Sci Plant Anal 37:155–162. https://doi.org/10.1080/00103620500403531
Savarese C, Cozzolino V, Verrillo M, Vinci G, De Martino A, Scopa A, Piccolo A (2022) Combination of humic biostimulants with a microbial inoculum improves lettuce productivity, nutrient uptake, and primary and secondary metabolism. Plant Soil 481 (1–2):285–314. https://doi.org/10.1007/s11104-022-05634-8
Siedt M, Schäffer A, Smith KEC, Nabel M, Roß-Nickoll M, van Dongen JT (2021) Comparing straw, compost, and biochar regarding their suitability as agricultural soil amendments to affect soil structure, nutrient leaching, microbial communities, and the fate of pesticides. Sci Total Environ 751:141607. https://doi.org/10.1016/j.scitotenv.2020.141607
Tahat MM, Alananbeh KM, Othman YA, Leskovar DI (2020) Soil health and sustainable agriculture. Sustainability 12:4859. https://doi.org/10.3390/su12124859
Tandon H, Cescas M, Tyner E (1968) An acid-free vanadate-molybdate reagent for the determination of total phosphorus in soils. Soil Sci Soc Am J 32:48–51. https://doi.org/10.2136/sssaj1968.03615995003200010012x
Ter Braak CJF, Verdonschot PFM (1995) Canonical correspondence analysis and related multivariate methods in aquatic ecology. Aquat Sci 57:255–289. https://doi.org/10.1007/bf00877430
Terefe T, Mariscal-Sancho I, Peregrina F, Espejo R (2008) Influence of heating on various properties of six Mediterranean soils. A Lab Study Geoderma 143:273–280. https://doi.org/10.1016/j.geoderma.2007.11.018
Venter ZS, Jacobs K, Hawkins HJ (2016) The impact of crop rotation on soil microbial diversity: a meta-analysis. Pedobiologia 59:215–223. https://doi.org/10.1016/j.pedobi.2016.04.001
Wang T, Hao Y, Zhu M, Yu S, Ran W, Xue C, Ling N, Shen Q (2019) Characterizing differences in microbial community composition and function between Fusarium wilt diseased and healthy soils under watermelon cultivation. Plant Soil 438:421–433. https://doi.org/10.1007/s11104-019-04037-6
Wani SP, Chander G, Sahrawat KL, Srinivasa Rao C, Raghvendra G, Susanna P, Pavani M (2012) Carbon sequestration and land rehabilitation through Jatropha curcas (L.) plantation in degraded lands. Agric Ecosyst Environ 161:112–120. https://doi.org/10.1016/j.agee.2012.07.028
Wei F, Feng H, Zhang D, Feng Z, Zhao L, Zhang Y, Deakin G, Peng J, Zhu H, Xu X (2021) Composition of rhizosphere microbial communities associated with healthy and Verticillium wilt diseased cotton plants. Front Microbiol 12:618169–618169. https://doi.org/10.3389/fmicb.2021.618169
Wolińska A, Kuźniar A, Gałązka A (2020) Biodiversity in the rhizosphere of selected winter wheat (Triticum aestivum L.) cultivars—genetic and catabolic fingerprinting. Agron 10:953. https://doi.org/10.3390/agronomy10070953
Yin H, Wheeler E, Phillips RP (2014) Root-induced changes in nutrient cycling in forests depend on exudation rates. Soil Biol Biochem 78:213–221. https://doi.org/10.1016/j.soilbio.2014.07.022
Zhao R, Wu K (2021) Soil health evaluation of farmland based on functional soil management—a case study of Yixing City, Jiangsu Province China. Agriculture 11:583. https://doi.org/10.3390/agriculture11070583
Zhao Y, Fu W, Hu C, Chen G, Xiao Z, Chen Y, Wang Z, Cheng H (2021) Variation of rhizosphere microbial community in continuous mono-maize seed production. Sci Rep 11:1544. https://doi.org/10.1038/s41598-021-81228-1
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Due acknowledgment goes to the National Research Foundation of South Africa for the award of UID132595 to OOB.
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AAA carried out the laboratory and fieldwork, handled the literature findings, executed all necessary analyses, interpreted the results, and prepared the manuscript. AEF provided technical input, assisted in result interpretation and OOB initiated the next-generation sequence research, helped shape the research, verified the analytical methods, secured funds for the study, proofread, commented on the manuscript at all stages, and supervised AAA and AEF.
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Core ideas
Physiochemical features of soil
Soil moisture content and water retention
Sequestration of carbon substrate
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Adedayo, A.A., Fadiji, A.E. & Babalola, O.O. Quantifying the Respiratory Pattern of Rhizosphere Microbial Communities in Healthy and Diseased Tomato Plants Using Carbon Substrates. J Soil Sci Plant Nutr 23, 6485–6496 (2023). https://doi.org/10.1007/s42729-023-01504-z
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DOI: https://doi.org/10.1007/s42729-023-01504-z