Lactic Acid Bacteria and Saccharomyces Boulardii Alleviate the Stunted Growth of Tomato under Osmotic Stress

Abstract

Osmotic stress through drought and salinity seriously threatens agriculture and our environment. We employed various probiotics to combat the osmotic stress in plants since they have been known to boost plant growth and productivity by inducing stress tolerance. In this study, we hypothesized that individual Lactic acid bacteria (LAB) strains such as Lactobacillus acidophilus (LA), Lactobacillus rhamnosus (LR), Bifidobacterium longum (BL), and Saccharomyces boulardii (SB) increase the growth of Solanum lycopersicum (tomato) in the presence of Sodium Chloride (NaCl). We evaluated the tomato growth by examining the germination rates of the seeds, as well as the weight, length, and morphology of sprouts cultured in Petri dishes. NaCl (0.1M) reduced the germination rate by 53% compared to the non-treated group, while the germination rate of the seeds treated with NaCl and individual strains (1 million CFUs/mL BL, LR, and SB) was 28% higher than those with NaCl alone. Additionally, incubation of the BL, LR, and SB to NaCl solution significantly (p<0.001) increased the length and weight of tomato sprouts compared to those grown in the NaCl-only solution. However, LA did not significantly increase tomato growth. Finally, each strain, including BL, LR, and SB, and 12 strains of LAB significantly (p<0.001) ameliorated the morphological change induced by NaCl. This finding suggests that not only LAB mixture but also individual probiotic strains, including BL, LR, SB, and LAB can help plants sustain in environments challenged by salinization and drought.

Introduction

Arid and coastal agricultural areas are considerably vulnerable to climate change, such as extreme heat and drought. The changes increase soil salinity through salt-water intrusion, shallow water tables, and reuse of degraded water¹. Increased salinization of arable land is likely to result in 30% land loss within the next 25 years and up to 50% by 2050¹’². Salinity imposes a significant threat on plant tissues³, resulting in reduced growth rate⁴. Salinity and drought exert their malicious effects mainly by disrupting the ionic and osmotic equilibrium of the cell. It is now well known that the stress signal is first perceived at the membrane level by the receptors and then transduced in the cell to switch on the stress-responsive genes for mediating stress tolerance³. The ability to adapt to changes in the osmolality of the external environment⁵  is of fundamental importance for the growth⁶ and survival of plants⁷. One effective solution to tolerate this stress has been known as bacteria that benefit plant growth, referred to as plant growth-promoting rhizobacteria (PGPR) or beneficial bacteria. These bacteria promote plant growth by colonizing the plant roots and are associated with the rhizosphere, making plant-microbe interactions possible⁸.

One of the most beneficial bacteria, called probiotics, helps plants reduce oxidative stress⁸, boost nutrient metabolism⁹, increase growth, and protect plants from multiple diseases¹⁰. Probiotics are live bacteria and yeasts that benefit the human body. Probiotic strains, such as Lactic acid bacteria (LAB), are live microorganisms naturally found in decomposing plants¹¹, fermented food, animals, the human body, and many other organisms¹². LAB, inclusive of all Lactobacillus and Bifidobacterium¹⁰ have been effective as biofertilizers, biocontrol agents¹¹, and biostimulants¹². LAB has been shown to play a critical role in plant disease control and plant growth directly by regulating the uptake of nutrients like phosphorus and potassium, fixing nitrogen, and producing plant hormones and siderophores. Indirectly, LAB could help with the reduction of phytopathogens through the production of a variety of antimicrobial compounds, including diketopiperazines, hydroxy derivatives of fatty acids, 3-phenylactate, hydrogen peroxide, pyrrolidone-5-carboxylic acid, diacetyl, and reuterin, and a defense mechanism by creating systemic resistance, and decreasing pathogen iron availability¹³’¹⁰.

Probiotic yeast Saccharomyces boulardii (SB) resides in plants such as mangosteens and lychee and produces many bioactive metabolites, which include antioxidant, antibacterial, antitumor, and anti-inflammatory properties in human¹⁴. SB exhibits stress tolerance during multiple conditions like osmotic shock by expressing stress genes and proteins¹⁵. They augment the survival of strains during the production and storage of the viable cell mass¹⁶. LAB can directly promote seed germination or plant growth in agricultural fields and aquaculture and alleviate various biotic stresses¹⁷’¹⁸. One of the most commonly found probiotics, LAB, has evolved several osmotic adaptive strategies to cope with this critical environmental factor¹⁹. Lactobacillus rhamnosus (LR), a strain of LAB, has been shown to withstand different stress factors including acidity and salt in food processing and the gastrointestinal tract¹⁶’²⁰..

Despite numerous studies showing that LAB and SB alleviate the biotic stress of animals and humans and help strains survive during osmotic stress from food processing²¹’²² , only few studies have found the effect of the individual probiotic strains on plants under osmotic stress²³’²⁴.

Additionally, we tried to find whether the protective effects of the individual LAB strains and SB are higher than those of the LAB mixture. In light of the recent information concerning the physiological responses of probiotic bacteria to the osmolality of the environment, probiotics could play a critical role in the salinity tolerance of plants¹⁵’¹⁶.

Therefore, we investigated how the individual LAB and SB affect the growth of Solanum lycopersicum in the presence of NaCl. We hypothesized that LAB and SB could protect tomato growth from osmotic stress as efficiently as LAB mixture since the probiotics increase its viability during osmotic stress and elevate plant growth. Our study begins with an effect of individual probiotic strains as well as an effect of salt on plants and then continues with a combined analysis of each strain of LAB and SB governing NaCl-induced stunted growth of tomato.

This study has provided the osmotic-stress tolerable effects of LA, BL, LR, SB, and 12 LAB strains in plants. Additionally, this unique experimental model used each strain and tomato plant that was available and affordable for execution. Besides, an osmotic challenge with 0.1M NaCl in tomatoes grown in Petri dishes occurred solely by focusing on the bacteria we treated without the effect of soil and soil bacteria. While Petri dishes lack the complexity of real-world soil environments, where interactions between plant roots, soil microbes, and nutrients are more dynamic, we think our experimental design, excluding complex factors like soil nutrients and soil bacteria, could clearly explain the sole effect of probiotics on tomato growth. We could further validate soil-based systems to understand how probiotics influence plant growth under more natural conditions. Ultimately, our study may contribute to our agriculture industry and environment by suggesting a potential for LAB to lessen the destructive stress of salt exposure and drought-driven salinity in California and other areas in the world.

Results

The effect of individual probiotic strains on tomato growth

In Petri dish culture, we tested the effect of individual probiotic strains on the growth of tomato sprouts (Figure 1). LA, BL, LR, SB, and LAB solutions at a concentration of one million CFUs/mL significantly increased the length and weight of tomato sprouts compared to the non-treated group. Sprouts grown in one million CFUs/mL of LA, BL, LR, SB, and LAB solutions for 21 days had an increase in the length of sprouts by 17%, 27%, 36%, 25%, and 39%, respectively, compared to the non-treated group. Additionally, the weight of sprouts grown in the one million CFUs/mL LA, BL, LR, SB, and LAB solutions for 21 days increased by 28%, 20%, 35%, 24%, and 29%, respectively, compared to the non-treated group. LAB displayed significantly (p<0.001) more increasing effects on the length and weight of the tomato sprouts than LA, BL, LR, and SB (Figure 1).

The effect of NaCl on tomato growth

To investigate the effects of various NaCl concentrations on seed germination and find out the effective concentration of NaCl on inhibition of tomato growth, we applied four concentrations (0.05, 0.1, 0.5, and 1 M) to each Petri dish. As the NaCl concentration increased, tomato seeds’ germination rates 14 days after placing the seeds (Figure 2) decreased significantly (p<0.001). While 94% of the tomato seeds germinated in the non-treated group, 60% and 44% of tomato seeds germinated in the presence of the 0.05 and 0.1 M NaCl solution, respectively. The application of 0.05 and 0.1 M NaCl significantly reduced the germination rate by 36% and 53%, respectively, compared to the non-treated group. However, none of the tomato seeds treated with 0.5 or 1 M NaCl germinated (Figure 2). Additionally, the length of each sprout treated with 0.05 and 0.1 M NaCl was significantly lower than those of the non-treated sprouts (p<0.001). The seeds grown in the Petri dish with 0.05 M and 0.1 M NaCl solution resulted in a 33% and 40% reduction in length of sprouts, respectively, compared to the non-treated group (Figure 2). After testing sprout length and germinated seeds frequency, we used the 0.1 M NaCl, closest to the 50% inhibition concentration, to test the effects of the probiotics on the tomato germination and growth.

The effect of individual strains on tomato growth at salinity

We cultured tomato seeds under either non-treatment or in various strains for three weeks in each Petri dish (Control: the non-treated group, ultrapure water only, NaCl: 0.1 M NaCl in ultrapure water, LA+NaCl:  0.1 M NaCl + 1 million CFUs/mL Lactobacillus acidophilus, BL+NaCl: 0.1 M NaCl + 1 million CFUs/mL Bifidobacterium longum in ultrapure water, LR+NaCl: 0.1 M NaCl + 1 million CFUs/mL Lactobacillus rhamnosus in ultrapure water, SB+NaCl: 0.1 M NaCl + 1 million CFUs/mL Saccharomyces boulardii in ultrapure water, andLAB+NaCl: 0.1 M NaCl + 1 million CFUs/mL LAB in ultrapure water). Seeds treated with both LAB and NaCl germinated significantly (p<0.001) faster and grew more than those in the NaCl-only group (Figure 3 and 4). The germination rate of tomato seeds grown with 0.1 M NaCl solution was 53% lower than the non-treated group 14 days after placing the seeds (Figure 3A and 3C). The germination rate of the seeds with BL+NaCl, LR+NaCl, and SB+NaCl solution significantly (p<0.001) increased by 28%, 28%, and 28%, respectively, compared to the NaCl-only group (Figure 3B and 3C).

Twenty-one days after placing the seeds, the length of sprouts grown with 0.1 M NaCl solution was 56% shorter than the non-treated group, while the length of sprouts grown with 1 million CFUs/mL LAB+0.1 M NaCl solution was 19% shorter than the non-treated group. Most interestingly, the sprouts grown with LAB+NaCl solution increased in their length by 85% compared to the ones grown with NaCl-only solution. The length of sprouts grown with BL+NaCl, LR+NaCl, and SB+NaCl solution significantly (p<0.001) increased by 36%, 45%, and 45%, respectively, compared to the NaCl-only group. Additionally, the weights of the sprouts grown with LA+NaCl, BL+NaCl, LR+NaCl, SB+NaCl, and LAB+NaCl solution increased by 27%, 31%, 34%, 30%, and 44%, respectively, when measured 21 days after placing than the plants grown with 0.1 M NaCl only solution. Tomato plants grown with LAB+NaCl solution significantly increased the growth compared to those grown with NaCl-only solution (p<0.001, one-way ANOVA test) (Figure 5). Adding 1 million CFUs/mL BL, LR, SB, and LAB solution significantly (p<0.001) reversed the NaCl-induced stunted growth. Incubation of the tomato sprouts with 1 million CFUs/mL of LAB solution with NaCl 0.1 M for three weeks increased the length and the weight of tomato sprouts compared to the NaCl-only groups by 85% and 44%, respectively (Figures 4B and 4C). In the presence of 0.1 M NaCl, the 1 million CFUs/mL BL, LR, SB, and LAB solution significantly (p<0.001) alleviated the NaCl-induced stunted growth. LAB displayed the most significant (p<0.001) increasing effects on the height and weight of the tomato plants compared to LA, BL, LR, and SB in the presence of 0.1 M NaCl (Figure 4).

Sprout Morphology

Osmotic pressure caused the reductions in turgor pressure within the cells that restricted cell expansion²⁵ and we observed more coil forms of sprouts in salt including solutions (Figure 5A). Therefore, we evaluated the effect of morphological changes, such as the number of coils in tomato sprouts in each group. The sprouts treated with 0.1 M NaCl revealed significantly (p<0.001) more coils than the ones treated with ultrapure water only. However, the co-application of 0.1 M NaCl and 1 million CFUs/mL of BL, LR, SB, and LAB significantly (p<0.001) reduced the number of coils in each sprout compared to the NaCl-only group (Figure 5B).

Discussion

In this study, we determined which individual strains of LAB and SB increased the growth of tomato seeds in Petri dishes without osmotic stress, and we found that one million CFUs/mL of BL, LR, SB, and LAB significantly (p<0.001) restored tomato growth in the presence of 0.1 M NaCl. The tested probiotic strains, such as LA, BL, LR, SB, and LAB, accelerated tomato growth compared to the non-treated group. In contrast, as the NaCl concentration increased, the germination rate of the seeds significantly (p<0.001) delayed, which indicated that the tomato sprout was sensitive to NaCl stress. Seawater contains approximately 3% NaCl, and in terms of molarity of different ions, Na+ is about 460 mM, and Cl- is 50 mM²⁶’²⁷. The NaCl concentration (0.1 M) we used may be similar to the NaCl amount in the seawater intrusion in coastal areas or shallow water tables. However, adding 1 million CFUs/mL LAB to the NaCl solution significantly increased the germination rate compared to the NaCl-only solution. The seeds grown in the LAB solution showed the most significant increase in germination rate compared to those in LA, BL, LR, and SB in the presence of NaCl. Since two individual strains of the LAB mixture, BL and LR exhibited a significant increase in tomato growth in the presence of salt we predict that BL and LR may be the specific strains driving the augmenting effect of the LAB mixture. We tested a limited number of LAB strains, and it is possible that strain-specific effects could vary with different probiotic formulations. Future research should expand the range of strains tested to assess whether certain LAB strains or combinations have superior effects on growth promotion and salt stress mitigation.

Elevated tomato growth with BL, LR, SB, and LAB in this experiment demonstrates the bacteria’s stress tolerance against salt in food processing and the gastrointestinal tract¹⁴’¹⁵. Another study found that LR withstood under 0.3 M NaCl osmotic shock¹⁶’²⁰. Considering that our concentration of NaCl (0.1 M) was lower than the one in the study, Lactobacillus could sufficiently tolerate the salt shock and help the tomato grow better than the salt-only solution.

Several mechanisms, like ion transport, osmotic adaptation, osmolyte synthesis, and antioxidative mechanisms, can be responsible for the growth and development of plants in saline environments²⁸’²⁹. Salt stress in tomatoes and soybeans has unregulated several GST genes, suggesting that they regulate redox homeostasis under salt stress conditions³⁰’³¹. Heat shock proteins GroEL and DnaK and the glycolytic enzymes glyceraldehyde-3-phosphate dehydrogenase, lactate dehydrogenase, enolase, phosphoglycerate kinase, and triose phosphate isomerase, as well as tagatose 1,6-diphosphate aldolase of the tagatose pathway may involve in the protective roles of probiotics³²’³³. We also found that yeast probiotics, SB isolated in plants, significantly increased tomato growth with and without NaCl. This suggests that yeast probiotics also boost plant growth under osmotic stress and that SB protects not only animal intestinal membranes but also plant membranes.

Importantly, we discovered that LAB with twelve strains, including LA, LR, and BL play a synergistic role in plant growth through the collective enhancement of certain strains. The complex responses to salt stress also contribute to the production of reactive oxygen species (ROS) that cause oxidative damage to membrane lipids, proteins, and nucleic acids, thus disrupting redox homeostasis²⁴’³⁴. LAB and SB could mitigate osmotic stress by reversing the decreased activities of antioxidant enzymes such as dismutase, catalase, ascorbate peroxidase, and glutathione reductase³⁵’³⁶.

In addition, salt tolerance may depend on the ability to regulate osmotic pressure through the accumulation of soluble carbohydrates and proline between roots and leaves and the improvement of plant salt tolerance. Several studies support that Lactobacillus can help tomato plants cope with salt stress by enhancing the plant’s osmotic adjustment ²²’²³. They increase the production of osmolytes such as proline, which help maintain water balance inside cells²³’³⁷. The contents of sugar and protein, including amino acid proline, may alter with salt and probiotics during tomato growth²²’²⁴. According to a study³⁴ applying Saccharomyces species to rice plants the colonization capacity of the PGPR strain was detected 100 times more abundant in the rice rhizosphere and this resulted in distinguishing increases in total carbon, total protein, total sugar, total amino nitrogen, total nitrogen, and phenol content in root exudate. The elevated release of the nutrients can increase photosynthetic activity and mineral uptake in dealing with water stress. Saccharomyces species have been shown to stimulate plant growth and enhance stress tolerance by producing bioactive compounds that boost plant defense mechanisms and growth. Saccharomyces can induce resistance to drought, salinity, and oxidative stress by modulating antioxidant systems and enhancing root biomass and overall plant performance under challenging environmental conditions.

Similarly, LAB can solubilize essential nutrients like phosphorus and potassium, making them more available to plants. They also enhance nitrogen fixation, which is crucial for plant development. LAB can improve nutrient availability from compost and other organic materials. LAB produces phytohormones, such as auxins and gibberellins, which promote root growth, increase nutrient uptake, and help plants cope with abiotic stresses like drought and salinity²² Furthermore, LAB produces antimicrobial compounds, which can help plants resist diseases by suppressing phytopathogens. These mechanisms collectively improve plant health and resilience under stress conditions, making LAB a valuable tool in sustainable agriculture systems³⁸.

Another study showed that the length, surface area, and volume of tomato roots (≤1 mm diameter) significantly decreased with the elevated NaCl concentration in soil.²⁵’³⁹. This morphological change in tomato plants was due to the reductions in turgor pressure within the cells that restricted cell expansion. Salt stress in tomatoes significantly alters root morphology, often leading to reduced root length, decreased root biomass, and a general decline in root surface area, which hampered water and nutrient uptake. Studies on salt-stressed tomatoes show that this stress condition induces changes in root architecture, including the thickening of root cells, reduction in lateral roots, and inhibition of primary root growth. These morphological changes are a plant’s attempt to adapt to high-saline environments by minimizing the uptake of toxic ions like sodium (Na+)​⁴⁰. Consistently, the coiled form of salt-treated sprouts in our experiments suggests that the osmotic stress altered the morphology of tomato plants and may also inhibit the tomato growth. Our results showed that the application of individual or collective strains of probiotic bacteria could ameliorate the inimical change of shapes of sprouts under osmotic stress. Our results suggest that various probiotics can offset the negative effect of NaCl stress on germination rates, length, biomass, and morphology. Therefore, either individual LAB or collective LAB, and SBcan offset the destructive effect caused by osmotic stress on tomato growth through stress tolerance.

Although the short-term growth effects of probiotics provides valuable insights into early-stage seedling development it is crucial to investigate the long-term impacts of probiotics on overall plant health, yield, and stress tolerance throughout the entire life cycle of the plant. Long-term studies could explore how probiotic treatments affect flowering, fruit set, and final crop yield in saline environments, which would be essential for determining the practical value of probiotics in agricultural production. Finally, future studies could include measuring antioxidant enzyme activities and the expression of the stress proteins such as GroEL and DnaK. The contents of nutrients in tomato sprouts and long-term impacts such as flowering, fruit bearing, and final crop yield in saline environments should be investigated. Our study demonstrated the eco-friendly applications of probiotics in saline conditions to improve soil structure, soil fertility, root development, and microbial treatment resulting in their effectiveness and scalability in real-world agricultural systems.

Materials and Methods

Preparation of tomato seeds and probiotics

We isolated seeds from ripe tomatoes (Solanum lycopersicum), washed and sterilized the seeds with ethanol, then washed the ethanol with sterile distilled water twice and thoroughly dried for one day at 20±5°C.⁴¹. We tested 30 seeds in each Petri dish under various conditions. We purchased various probiotic capsules of the individual bacteria, LAB and SB. One capsule of Bifidobacterium longum (Supersmart) included 6 billion CFUs BL. One capsule of LA (Nature’s Bounty Acidophilus Probiotic) contained 1 billion CFUs LA. One capsule of LR (Culturelle)contained 10 billion CFUs LR (GG). Moreover, one capsule of SB (Florastor) included 5 billion CFUs SB (CNCMI-745). Finally, One capsule of LAB probiotics (TruNature) contained 10 billion CFUs of 12 different LAB strains (Lactobacillus rhamnosus GG, Lactobacillus paracasei, Lactobacillus acidophilus, Lactobacillus casei, Lactobacillus plantarum, Lactobacillus reuteri, Lactobacillus salivarius, Bifidobacterium lactis, Bifidobacterium infantis, Bifidobacterium bifidum, Bifidobacterium breve, Bifidobacterium longum). We diluted the final solutions from each capsule into 1 million CFUs/mL using ultrapure water (Maxtite) in Petri dishes.

The effect of individual probiotic strains on tomato growth

We tested five different groups (Control: ultrapure water, LA: 1 million CFUs/mL LA in ultrapure water, BL: 1 million CFUs/mL BL in ultrapure water, LR: 1 million CFUs/mL LR in ultrapure water, SB: 1 million CFUs/mL SB in ultrapure water, and LAB: 1 million CFUs/mL LAB in ultrapure water) and counted the number of sprouts coming out of the seeds. We measured the length (in cm) from the tip to the end of each sprout with a ruler and the weight of dried sprouts 21 and 28 days after placing the seeds using a 300 x 0.001g Precision Balance (U.S. Solid 0.001g 1mg Digital Analytical Balance Precision Scale for Laboratories). We repeated each test three times for accuracy.

The effect of NaCl on tomato growth

We carried out the seed germination assays for osmotic stress according to the USEPA guidelines⁴². The Petri dish culture of tomato followed the procedure listed in a reference.⁴². In each Petri dish, we placed 30 seeds from tomato with 30 mL of NaCl solution in various concentrations (0, 0.1, 0.5, and 1M) in ultrapure water for the seed germination assay. We placed the sealed Petri dishes in a germination incubator at 25±5°C, with 30-40% humidity (ThermoPro TP50 Digital Hygrometer). After two weeks, we counted the number of germinated seeds and measured the lengths of the sprouts in cm in each Petri dish. When we observed 90% of the control seeds’ sprouts had grown at least 20 mm long, we completed the germination test. Once we determined the NaCl concentration of optimal osmotic stress, we applied individual Lactic acid bacteria (LAB) such as LA, BL, and LR, as well as a mixture of 12 strains of LAB to either ultrapure water only solution or NaCl solution, both in sterile Petri dishes.

The effect of individual strains on germination rate and tomato growth at salinity

We added LA, BL, LR, SB, and LAB from single capsules at a concentration of 1 million CFUs/mL to 0.1 M NaCl solutions. Then, we added 30 tomato seeds to each Petri dish. We cultivated the seeds of each group with a final amount of 30 mL of its respective solution. We tested six different groups (Control: ultrapure water, LA+NaCl: 1 million CFUs/mL LA and 0.1 M NaCl in ultrapure water, BL+NaCl:  1 million CFUs/mL BL and 0.1 M NaCl in ultrapure water, LR+NaCl: 1 million CFUs/mL LR and 0.1 M NaCl in ultrapure water, SB+NaCl: 1 million CFUs/mL SB and 0.1 M NaCl in ultrapure water, and LAB+NaCl: 1 million CFUs/mL LAB and 0.1 M NaCl in ultrapure water) and counted the number of germinated sprouts. We measured the length (in cm) from the tip to the end of each sprout with a ruler and the weight of dried sprouts from the Petri dish 21 days after placement of the seeds with a 300 x 0.001g Precision Balance. We repeated each test three times for accuracy.

Effect of individual strains on sprout morphology at salinity

We examined the number of coils in tomato sprouts in each group. We dried the sprouts treated with 0.1 M NaCl and the co-application of 0.1 M NaCl and 1 million CFUs/mL of BL, LR, SB, and LAB and measured the number of coils in each sprout 21 days after placing the seeds in Petri dishes. We repeated each test three times for accuracy.

Statistical Analysis

The data represent the average of each measurement (n=3). The one-way ANOVA (Analysis of Variance) was used to analyze the significance of comparing multiple groups. Post Hoc Tukey HSD (Honestly Significant Difference) test was followed to facilitate pairwise comparison within our ANOVA data. Statistical significance was determined at the level of p<0.05. The statistical analysis was conducted in Socscistatistics.com.

Acknowledgments

We would like to thank Ms. Karen Saxena of Gunn High School who continued to support my research. Also, we truly appreciate Alan Lee, who provided countless suggestions when compiling and presenting results.

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