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Pseudomonas ZY-1 and Bacillus FY-1 protecting the rice seedlings from the harm of Pseudomonas aeruginosa via indirect seawead lysis

BMC Microbiology volume 24, Article number: 375 (2024) Cite this article

Abstract

The local ecosystems, fishery and human health are all threatened by water blooms, so effectively controlling water blooms has become an urgent and challenging issue. Biological control of water blooms is given priority due to its low cost, high efficiency and environmental friendliness. In this study, Pseudomonas ZY-1 and Bacillus FY-1, two highly-effective algicidal bacteria strains which are able to indirectly lyse algae by separating and screening from the vigorous water body in the paddy alga of Northeast China were obtained. The two bacterial strains have stronger ability to lyse alga in the bacterial liquid concentration of 106 CFU/ml, and the alga-lysing rate on 7 d reached 84.03% and 83.11% respectively. The active substance secreted by ZY-1 is not sensitive to the changes of temperature and pH value, while as FY-1 cell-free filtrate is not stable in high temperature above 50 ℃ and pH of 5, it requires the sun light to have the algaecidal effect. The cell-free filtrates of strains ZY-1 and FY-1 had the best lysis effect on Microcystis aeruginosa cells, and the chlorophyll a content of algae decreased to 0.13 ± 0.02 mg/L and 0.14 ± 0.03 mg/L respectively and the Fv/Fm of Microcystis aeruginosa decreased by 97.22% after 7 days. The algaecidal process of ZY-1 and FY-1 may be that the cell-free filtrate inhibits the photosynthesis of Microcystis aeruginosa, and meanwhile it avoids the regeneration and repair of photosynthesis of algal cells by affecting the gene expression and damaging the repair system of algal cells, so the membrane lipid peroxidation is exacerbated and then the membrane of algal cells is broken, the algal cells can’t do normal life activities, and finally the algal cell would be killed. The rice seedlings in the algal liquid treatment group are short and show root dysplasia, few roots and brown roots. After treated with cell-free filtrate of ZY-1 and FY-1, the oxidative damage of the rice is obviously reduced, and the harm from Microcystis aeruginosa is reduced, which has the repair effect to the roots of rice seedlings and its aboveground growth. The cell-free filtrate of FY-1 works better than ZY-1. The bacteria strains of ZY-1 and FY-1 have the indirect algaecide trait, which makes them the potential environmentally-friendly algaecidal bacteria and they show broad application in the agricultural production and the control of water blooms.

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Introduction

The nutritious water body leads to composition and distribution imbalance of species in the aquatic ecosystem. With the unique growth advantage, the planktonic algae begins to reproduce in quantities, and finally the harmful water blooms form. The reasons of the formation of water blooms involve many aspects, among which nutritional overload and the global climate warming have become the key reasons [1]. The research of Hans shows that nutritional pollution is the main driving factor to the blue-green algal and other harmful algal proliferation. The usability of phosphorus and nitrogen is the important elements of facilitating the growth of water body in the aquatic ecosystem [2], and the agricultural runoff, sewage disposal and atmospheric sedimentation can all cause the excessive phosphorus and nitrogen. Diatom has disproportionate large storage bulbs, and prefers to grow in the environment rich in nitrogen and phosphorus [3], and the shortage of nutrition inhibits the growth of diatom [4]. The climate change is another factor closely linked to the alga growth, and the growth season and temperature of different kinds of alga varies. Dinoflagellate grows well in the temperature of more than 10 ℃, and 20–27℃ is its optimum temperature [3]. Michael found that the volume of algal organism will increase with the rising of temperature, especially Blue-green alga and Microcystis, they change obviously [5]. The problem of water blooms is increasingly prominent. It has a negative impact on the environment, human’s economy and life. Farabegoli et al. reported that the economic loss due to Paralytic Shellfish Poisoning resulted from Dinoflagellate outbreak reaches more than 60,000 dollars in Alaska [6]. Microcystis aeruginosa is the most common factor that causes the water blooms [7], and its secretion microcystin can result in DNA damage, acute liver failure and even the death of animals and human. If water blooms precipitate for a long period, the toxin released will further affect and endanger the health of animals and humans [8].

The biological control of water blooms is a kind of ecological restoration technology based on the interaction of bacteria and alga, because it can effectively adjust the microalgae composition, alga abundance and physical and chemical processes in water environment, and meanwhile have the traits of low cost and environmentally friendly, attracting much attention [9]. Researchers have separated and obtained multiple kinds of algaecidal bacteria that can kill the harmful alga or inhibit its growth, most of which are Bacteriophage, Flavobacterium, Bacteroides or Proteobacteria [10]. Among these, the algaecidal bacteria to blue-green alga are mainly Bacillus (31.1%), Proteus (24.5%) and Pseudomonas (8.6%) [11]. Liu separated and obtained Bacillus sp. Sp34 in Dianchi lake of China which exerts the potent algaecidal effect and inhibition through secreting heat-resistant and acid-alkali resistant substances [12]. Zheng obtained the Pseudomonas Ps3 whose zymotic fluid can damage the transverse sulcus of Gymnodinium catenatum and leads to cytoplasmic liquefaction and the loss of basic cellar function, causing the death of algae [13].

Returning straw to the field is a method of piling up straw that can not be used directly as fodder and putting it into the cultivated soil after it has decomposed, so as to increase soil fertility and improve soil properties. Returning straw to the field can not only reduce the environmental stress, but can increase markedly the surface soil nutrition [14], so it is a main rice cultivation measure in the Northeast of China at present. With the combination of long-term use of fertilizer, it makes the paddy soil much abundant in nitrogen and phosphorus. Because of the optimal nutrition and temperature, the paddy alga is easy to excessively reproduce, so it not only competes with rice seedlings for nutrition and oxygen, but its feature of shading can cause the temperature of water body slowly rising, severely affects the ecological environment of paddy and the rice production. But the problem of excessive reproduction of paddy alga has not yet attracted people’s attention. Therefore, separating and obtaining the environmentally-friendly and highly-effective algae-lysing strains has an important application value of reducing the hazard brought by harmful alga to rice, and meanwhile provides precious bacteria strain resource for the comprehensive control of water blooms. In this study, two bacteria strains (Pseudomonas sp. ZY-1 and Bacillus sp. FY-1) that are highly effective algicidal bacteria and can indirectly solubilize alga were separated. Then we analyzed the effect and mechanism of algae-lysis and found that the cell-free filtrate of the two strains can both relieve the harm of Microcystis aeruginosa to the rice seedlings, further effectively reducing the oxidative damage to roots and facilitating the plant growth, and the summary diagram of experimental design is shown in Supplemental Fig. 1.

Materials and methods

The separation and determination of algicidal bacteria

The cultivation of Microcystis aeruginosa

Microcystis aeruginosa FACHB-918 was chosen as the experimental alga species (purchased from The Freshwater Algae Culture Collection at the Institute of Hydrobiology in Wuhan of China). Microcystis aeruginosa FACHB-918 was transferred at the proportion of algal fluid and BG11 medium of 1:10 (v/v), and then was put in the illuminating incubator with the temperature of 25℃, light intensity of 1500 lx and light-dark ratio of 14 h:10 h and cultivated. The flask was manually shaken for 2–4 times every day. When the concentration of culture medium reached OD680 = 0.6 ± 0.02, the medium could be used for the following algaecidal experiments, meanwhile when the light intensity was adjusted to 2000 lx, the cultivation was continued, and when the concentration reached OD680 ≈ 0.8, the subculture would be conducted under the same culture conditions as the above.

The sampling and the separation of bacteria strains

The water sample was collected from the paddy in spring in Jilin province (North latitude 43°05’~45°15’; East longitude 124°18’~127°05’), when the paddy algae was excessively reproducing. The water sample of 100 µL was collected, and diluted with the concentration gradient dilution method, then applied on Luria-Bertani (LB) culture medium plate [15], and cultivated in the constant temperature incubator with the temperature of 30 ℃ until colonies grew, and then single colonies with different colors and shapes were chosen followed by the separation with streak plate method until the grown colonies were completely identical.

Co-culture of algaecidal bacteria

The single colonies separated and obtained in 2.1.2 were transferred into the fluid medium LB of 10 ml under 30 ℃, 180 rpm and conducted shaking culture for 12 h. Then the light absorption value at 600 nm of the bacteria fluid was determined every 1 h, and then drew the growth curve. The bacteria fluid at OD600nm = 0.8 was taken as the seed fluid for the following experiments (unless otherwise specified, the preparation of seed fluid of bacteria strains is the same as the above). The co-culture was conducted in the proportion of 1:10 (v/v) of the seed fluid of bacteria strain and algal liquid, with the temperature of 25℃, light intensity of 2000 lx and light-dark ratio of 14 h:10 h. LB of the same volume was transferred as control, and three repetitions were set in each treatment group. The flask was manually shaken for 2–3 times every day and the change of color was observed. Meanwhile, the content of chlorophyll a of alga was determined every day and the algae dissolution rate was calculated. Acetone repeated freeze-thaw extraction method was used to determine the content of chlorophyll a and see the literature for detailed steps [16], the bacteria strain that yellows the algal fluid and reduces the content of chlorophyll a was preliminarily determined as algaecidal bacteria strain. At the same time, to determine the bacteria growth in the co-cultivation system of algal bacteria, we took 100 µL of co-culture medium to apply evenly on the solid LB medium after gradient dilution of it, then cultured it in 30 ℃ for 12 h and then counted the number of colonies.

The determination of the algae-lysing threshold of bacteria strains

  1. (1)

    The determination of algae-lysing rate with different initial bacterial liquid [17]: the algaecidal bacteria seed liquid was taken and LB was used to adjust the concentrations of bacterial liquid as 1 × 104, 1 × 105, 1 × 106 and 1 × 107 CFU/mL, then 1 ml of the bacterial liquid was added into 9 ml of algal liquid to be co-cultured. The co-cultured liquid was taken on 5 d and 7 d and then the number of algal cells was determined with hemocytometer. The algaecidal rate was calculated as follows: R= (C0-C1) / C0 × 100%, R represents algaecidal rate; C0 represents the number of algal cells in the control group, C1 is the number of algal cells in the treatment group.

  2. (2)

    The determination of algaecidal rate of the bacterial liquid at different initial concentrations of algal liquid: 1 ml of algaecidal bacterial seed liquid was respectively added to algal liquid with concentrations of 1 × 105, 1 × 106, 1 × 107 cells/mL. The algaecidal rate was determined on 5 d and 7 d with the same method as above.

The identification of molecules in the algaecidal bacteria

The genome DNA of the bacteria was extracted by using bacterial genome DNA extraction kit (Solarbio). The universal prime 27 F and 1492R of 16SrDNA were chosen to amplify the gene segments of 16SrDNA. PCR products were recycled and then sequenced (Sangon Biotech (Shanghai) Co., Ltd.). The sequences obtained were compared in NCBI database and the phylogenetic tree was built via Neighbor-Joining of MEGA 7.0.

The analysis of algae-lysing mode of the bacteria strains and traits of the algae-lysing substance

The determination of algae-lysing mode of bacteria strains

  1. (1)

    The determination of cell-free filtrate of bacteria strains and algaecidal rate of washed cell: 12,000 rpm of the seed liquid of bacteria strain was taken, and then centrifugated for 2 min followed by the supernatant being taken. The cell-free filtrate was obtained by filtrating with 0.22 μm filter membrane. Then it was washed and precipitated with LB liquid for three times and the washed cells were obtained (following the same). 1 ml of the cell-free filtrate or washed cells equivalent to 1 ml of culture medium was respectively added to 9 ml of algal liquid and put into the illuminating incubator with the temperature of 25 ℃, light intensity of 2000 lx and light-dark ratio of 14 h:10 h to co-culture. The number of the remaining alga cells was counted with the hemocytometer on 7 d and the algaecidal rate was calculated with the method same as 2.1.4.

  2. (2)

    Scanning electron microscope (SEM) of alga cells findings: This work was performed by reference to literature [18], and the detailed steps are as follows: 1 ml of the co-culture liquid was taken on 7 d, then it was centrifugated at the rate of 12,000 rpm for 2 min, then the supernatant was discarded. The cells was resuspended with 1 mL 2.5% of the glutaraldehyde and then was put in fridge with the temperature of 4 ℃ to stabilize for 24 h; then the liquid was centrifugated at the rate of 12,000 rpm for 5 min, the supernatant was discarded, PBS solution with the pH = 7.0 was used to wash cells for three times, then the liquid was centrifugated at the rate of 12,000 rpm for 5 min, and the supernatant was discarded. The liquid was dehydrated with 30%, 40%, 50%, 60%, 70%, 80%, 90%, 95%, 100% of ethanol solution for 10 min respectively. Then the supernatant was discarded and the remaining liquid was added into the vacuum concentration rotary evaporator to evaporate for 1 h. Then the sample was applied evenly on SEM stage, and observed using the field emission scanning electronic microscope HitachiSU8010 (Hitachi, Japan).

Optimization of the algaecidal rate of algal substances

  1. (1)

    The determination of algaecidal rate of cell-free filtrate of the algaecidal bacteria during different growing phases: the bacteria was cultured to the lag phase, Logarithmic growth period and stationary phase with the culture methods the same as 2.1.3. The cell-free filtrate was prepared and 1 ml of it was added into 9 ml of algal liquid to culture.

  2. (2)

    The determination of algacidal rate of the bacteria’s cell-free filtrate in different temperature: 1 ml of the cell-free filtrate in logarithmic growth period was taken and added into 9 ml of algal liquid to culture, and then put it into the illuminating incubator with the temperature of 0 ℃、25 ℃、50 ℃、75 ℃ and 100 ℃, liand light-daght intensity of 1500 lx rk ratio of 14 h:10 h to culture for 7 d. Then the survival algal cells number was counted to calculate the algaecidal rate.

  3. (3)

    The determination of algaecidal rate of cell-free filtrate under different PH: 1 ml of cell-free filtrate in logarithmic growth period was taken and added into 9 ml of algal liquid. Then 0.1 ml of HCL and NaOH was added to adjust pH to 3, 4, 5, 6, 7, 8 and 9, other culture conditions were the same as (1), and then the survival algal cells was counted to calculate the algaecidal rate after 7 d.

  4. (4)

    The determination of algaecidal rate of the cell-free filtrate in different illumination time: 1 ml of cell-free filtrate in logarithmic growth period was added into 9 ml of algal liquid and put under the conditions of full exposure, all darkness and light-dark ratio of 14 h:10 h, 25 ℃ and light intensity of 1500 lx to culture. The survival algal cell number was counted to calculate the algaecidal rate after 7 d.

Algaecidal mechanism test

The determination of photosynthesis index

Cell-free filtrate and the algal cells were cultured at the ratio of 1:10 (v/v), and then the samples at 0 d, 3 d, 7 d were taken. After that, the chlorophyll fluorescence parameters was determined using portable plant efficiency analyzer ( PEA, HansatechR, U.K.). Exciting laser intensity was 50% of the maximum intensity (1500 µE− 2·S− 1). The dark adaptation is not less than 15 min with recording time as 5 s and the determination was conducted under the room temperature. The ratio of variable fluorescence (Fv) and maximum fluorescence (Fm) expresses the Photosynthetic efficiency.

The determination of antioxidant activity of the algal strain

  1. (1)

    The preparation of the solution to be tested: 10 ml of cell-free filtrate was taken and co-culture with algal liquid. Then the mix was broken with the ultrasonic cell breaker for 5 min with the ultrasound time of 5 s and interval of 5 s. After that, the mix was centrifugated at the rate of 4000 rpm for 10 min under 4 ℃ and the supernatant was used for the determination of antioxidant index.

  2. (2)

    The determination of antioxidant parameters: the activity of superoxide dismutase (SOD) was determined with WST-1 method, peroxidase (POD) and catalase (CAT) with colorimetry and ascorbate peroxidase (APX) with ultraviolet colorimetric method. The content of Malondialdehyde (MDA) was determined with TBA method. The above tests were all conducted with test kits (Nanjing Jiancheng Biotechnology Research Institute (China)).

RT-qPCR test of algal cells’ relative gene

The cell-free filtrate and algal cells were cultured at the ratio of 1:10 (v/v), and 10 ml of the co-cultured liquid was taken at 9 h,18 h,36 h,72 h respectively. After that, the liquid was centrifugated at the rate of 12,000 rpm for 10 min under 4 ℃. Then the precipitation was ground in the liquid nitrogen. The total RNA of algal cells was extracted with Trizol method. gDNA was removed with PerfectStart®UniRT&qPCRKit (Beijing TransGene Biotech Company, China) and reverse transcription test and qPCR tests of psbA1, psbD1, rbcL, recA were conducted with 16 S rDNA as the internal reference gene. The gene level was calculated following 2–ΔΔCt method.

The impact testing of cell-free filtrate on the rice growth under stress of Microcystis aeruginosa

The rice seeds were put in water and then cultivated under the room temperature until germinated. After that, the seeds were planted in soil evenly and grew in 28 ℃ for 15 d. When the height of seedlings grew to 10 cm, the plants grow evenly were chosen to transfer to nutrient solution of 1/2 Hongland to cultivate. The algal liquid at OD680nm = 0.6 ± 0.02 was taken and then its density was adjusted to 106 cells/ml with BG11 medium. ZY-1 and FY-1 were added into the medium, algal liquid and the cell-free filtrate treated by ZY-1 and FY-1 with the cell density of 106 CFU/ml at the ratio of 10:1:0.1 (v/v/v). The culture medium and alga liquid of the corresponding volume was added into Algal and cell-free filtrate treated by ZY-1 and FY-1 was replaced with LB. CK1 was cultivated with nutrient solution of 1/2 Hongland of the same volume, and the culture medium of the corresponding volume, BG11 medium and LB medium was added into CK2. The samples were continued to cultivate for 15 d, and then were taken to determine the relative indexes. The root scanner Epson Expression V800 photo (Japan) was used in combination with root analyzer WinRHIZO (China) to analyze the root length, number of root tips, root surface area and root volume of the rice plants. SOD, POD, CAT and MDA of rice plants were determined following the method in the reference [19].

Results and analysis

Screening and identification of algaecidal bacteria

The culture medium of bacteria strain ZY-1 and FY-1 was co-cultured respectively with Microcystis aeruginosa FACHB-918 for 7 d. From Fig. 1A, the bacteria strains made the algal liquid yellow at different extent, 7 d later, showed no green. So in preliminary view, the two strains had the algae-lysing ability. The identification test of 16 S rDNA found that ZY-1 is Pseudomonas (Pseudomonas helmanticensis) (see the Supplemental Fig. 2); FY-1 is Bacillus (Bacillus altitudinis) (see the Supplemental Fig. 3). The algae-lysing ability of ZY-1 and FY-1 was determined in co-culture test of alga and bacteria, and the results shows in Fig. 1B. The content of Chlorophyll a in the co-culture system of alga and bacteria of ZY-1 and FY-1 was turned to the lowest on 7 d, which shows that the two bacterial strains both have obvious algae-lysing effect.

Fig. 1
figure 1

Algae-lysing effect of ZY-1 and FY-1 co-cultured with Microcystis aeruginosa. (A. Algal lysis effect of ZY-1 and FY-1 co-cultured with Microcystis aeruginosa on the 7th day; B. Chlorophyll A change curve of ZY-1 and FY-1 co-cultured with Microcystis aeruginosa for 7 days; C1. algaecidal rate of ZY-1 strain with different densities co-cultured with Microcystis aeruginosa for 5 days and 7 days; C2. algaecidal rate of different density algal cells co-cultured with ZY-1 strain for 5 and 7 days; D1. algaecidal rate of FY-1 strain with different density co-cultured with Microcystis aeruginosa for 5 days and 7 days; D2. algaecidal rateof different density algal cells co-cultured with FY-1 strain for 5 days and 7 days) Note : Different lowercase letters a, b and c indicate significant differences based on p < 0.05

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Under different bacterial density, the algae-lysing effect of ZY-1 (Fig. 1C1) and FY-1 (Fig. 1D1) was increased with the initial density of bacterial liquid. When the initial density of bacterial liquid of the two strains was 1 × 106 CFU/ml, the algaecidal rate reached the highest on 7d. When the initial density of bacterial liquid was 1 × 107 CFU/ml, the algaecidal rate was not obviously increased compared with that when initial density of bacterial liquid was 1 × 106 CFU/ml. So bacterial density of 1 × 106 CFU/ml was the algaecidal threshold of ZY-1 and FY-1 and the algacidal rate on 7 d was respectively 84.03% and 83.11%. The bacterial density of 1 × 106 CFU/ml was chosen to be the initial bacterial density, and we explored the algae-lysing effect under different initial algal cell density. The algae-lysing effect of ZY-1 (Fig. 1C2) and FY-1 (Fig. 1D2) are both decreased with the increase of the inital algal liquid.The algaecidal rate of two bacterial strains was the lowest when the concentration of algal liquid was 107 cells/ml. Therefore, when the density of algal liquid is 107 cells/ml, it is the algae-lysing threshold of ZY-1 and FY-1 and if the density is lower than 107 cells/ml, the two bacterial strains both have relatively high algaecidal rate.

The optimization of algaecidal mode of ZY-1 and FY-1 and the algaecidal rate of cell-free filtrate

The algaecidal rate of the cell-free filtrate of ZY-1 and FY-1 and the washed cells was determined. Then the algaecidal mode of the two strains of algaecidal bacteria were explored and it was found that the algaecidal rate of cell-free filtrate of ZY-1 (Fig. 2A) and FY-1 (Fig. 2B) and Microcystis aeruginosa reached respectively 82.18% and 81.24% after 7d of co-culture, and the algaecidal rate of washed cells was only 15.31% and 12.15% respectively. Algaecidal rate of the cell-free filtrate of ZY-1 and FY-1 is similar to that of bacterial zymotic liquid, while the algaecidal rate of washed cells is obviously lower than that of bacterial zymotic liquid, demonstrating that the two bacterial strains lyse alga indirectly. The scanning electron microscope further proves this result, for the algal cells in the control group is in the division phase in which the cells are full with smooth surface and without flaw or wrinkle. In SEM field of algal cells after treated with ZY-1 and FY-1, there is no obvious bacterial cells and the algal cells show surface wrinkle and damage at different extent (Fig. 2C).

Fig. 2
figure 2

Identification of algaecidal modes of ZY-1 and FY-1 and optimization of algaecidal conditions of cell-free filtrate. (A. algaecidal rate of scrubbed cells and cell-free filtrate of ZY-1; B. algaecidal rate of washed cells and cell-free filtrate of FY-1; C. Sem photos of Microcystis aeruginosa under different treatments; D. algaecidal rate of cell-free filtrate under different temperature conditions; E. algaecidaln rate of cell-free filtrate under different pH conditions; F. algaecidaln rate of cell-free filtrate in different growth stages of strains; G. algaecidal rate of cell-free filtrate under different light conditions) Note Different lowercase letters a, b, c, d, e and f indicate significant differences based on p < 0.05

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The algaecidal conditions of cell-free filtrate of two bacterial strains were optimized. Figure 2D shows that under different temperature, cell-free filtrate of ZY-1 and FY-1 show different algaecidal effects. ZY-1 shows high algacidal effect under 25–50 ℃ and over 60% under 0-100℃. The cell-free filtrate of FY-1 shows fair algaecidal effect in the temperature below 50 ℃. The algaecidal effect is lower than 60% when the liquid is treated in 75 ℃ and 100 ℃ and it is obviously low when the liquid is treated in 100 ℃ and the algaecidal rate is only 37%. Treated under different pH, the cell-free filtrate of ZY-1 shows fair algaecidal effect when pH is 4–9 (Fig. 2E), and when PH is 3, the algaecidal rate is obviously lower than that at other pH values, but over 50%. FY-1 shows best algacidal effect when pH is 6–8, but when pH is 4, 5 or 9, the algaecidal effect is decreased and it is lower when pH is 3. This result suggests that the active substance released by ZY-1 is not sensitive to the change of temperature and pH, while the cell-free filtrate of FY-1 is not stable under high temperature and pH below 5.

The algaecidal rate of cell-free filtrate was determined when ZY-1 and FY-1 is in lag phase, Logarithmic period and stable phase. The result is shown in Fig. 2F, that is the algaecidal effects of cell-free filtrate in lag phase of the two strains are both lower than 50%, but the algaecidal effects in logarithmic period and stable phase are both over 80%. The ability of two strains of cell-free filtrate to remove algae under full light, dark light cycle, and all dark conditions was studied and shown in Fig. 2G. The results show that lighting conditions have a greater impact on algal cells. The algaecidal rates of cell-free filtrate of the two bacterial strains in full-illumination and dark-light cycle are both higher than that in all dark condition. The cell-free filtrate of the two bacterial strains has the algaecidal effect only under proper light condition.

The algaecidal mechanism

The impact of cell-free filtrate of ZY-1 and FY-1 on photosynthesis

The above study indicates that light is the necessary condition of cell-free filtrate of ZY-1 and FY-1 lysing alga. It can be inferred that perhaps cell-free filtrate of bacteria causes the cell lysis and death by inhibiting the photosynthesis of Microcystis aeruginosa. Therefore, to further determine the impact of cell-free filtrate on the photosynthesis of algal cells, the photosynthesis indexes of co-culture of cell-free filtrate and algal cells on 3 d and 7 d were determined. Results show that maximum light quantum yield (Fv/Fm) is slightly higher on 3 d than that on 0 d and 7 d, and the Sun/Solar-induced Chlorophyll Fluorescence (φE0), chlorophyll fluorescence parameters (PiAbs) and light-induced Oxidation-Reduction Potential (ψ0) has the tendency of increasing with time going, which is because that the algal cells grow normally and increase in number. But compared with the control group, Fv/Fm (Fig. 3A), φE0 (Fig. 3B) and PiAbs (Fig. 3C) of cell-free filtrate treated with ZY-1 and FY-1 are all lower on 3 d and 7 d, the values of treated groups are close to 0 on 7 d, and all indexes of FY-1 cell-free filtrate are all lower much on 3 d and 7 d than that of ZY-1. The chlorophyll-releasimg rate (φD0) (Fig. 3D) of the control group is not changed markedly on 0 d, 3 d and 7 d, while those of cell-free filtrate treated by ZY-1 and FY-1 are obviously higher than that of control group and that on 3 d is higher than that on 7 d. ψ0 (Fig. 3E) of cell-free filtrate of ZY-1 and FY-1 is lower than that of control group, but ψ0 on 7 d is higher than that on 3 d. It indicates the cell-free filtrate of ZY-1 and FY-1 has impact on the algal cells’ photosynthesis system. The photosynthesis effect of algal cells are reduced, indicating that the photosynthesis system function is inhibited and the energy transfer and organic substance accumulation are suppressed, then the alga can’t grow normally.

Fig. 3
figure 3

Effects of cell-free filtrate of ZY-1 and FY-1 on photosynthetic characteristics of algal cells. (A. Fv/Fm; B. φE0; C. PiAbs; D. φD0; E. ψ0 ) Note : Different lowercase letters a, b and c indicate significant differences based on p < 0.05

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The change of algal cells’ antioxidant system by the cell-free filtrate of ZY-1 and FY-1

The algae-lysing bacteria affect the photosynthesis, mostly accompanying the oxidative damage of algal membrane, so the antioxidant enzyme system of algal cells was determined. On the four time points between 0 and 7 d, in control group, except that T-AOC is tend to increase slightly, POD, CAT, SOD, APX and MDA don’t change obviously with the time changes. After the cell-free filtrate of ZY-1 and FY-1 is co-cultured with algal cells, POD (Fig. 4A) of algal cells reaches the highest on 5 d, and then is obviously lowered. CAT (Fig. 4B), SOD (Fig. 4C), APX (Fig. 4E) and POD tend to change in the same way. The result of T-AOC (Fig. 4D) of algal cells shows that T-AOC activity of cell-free filtrate of ZY-1 and FY-1 reaches the highest on 3 d, and obviously higher than the control group, is gradually decreased after 3 d and the activity of T-AOC on 5 d and 7 d is obviously lower than that of the control group. When cellar organs are damaged under aging or adversity, the membrane lipid peroxidation will occur. The final decomposition products is MDA (Fig. 4F) whose content can reflect the extent of damage of the organism in adversity as an instant method. In the ZY-1 and FY-1 treated group of cell-free filtrate, we detected the content of MDA is gradually accumulated between 0 and 7 d, indicating that the algal cells were affected by membrane lipid peroxidation continuously.The content of MDA at 7 days increased to 0.49 ± 0.01 nmol/mg protein and 0.48 ± 0.02 nmol/MG protein, respectively. Membrane lipid peroxidation occurred, which activated the antioxidant enzyme system of algae cells. So it comes to conclusion that the cell-free filtrate of ZY-1 and FY-1 damages the membrane lipid peroxidation of algal cells, further causing the broke of cells, which is another reason of highly-effective algae-lysing of the two bacterial strains.

Fig. 4
figure 4

Effect of cell-free filtrate of ZY-1 and FY-1 on antioxidant system of algal cells. (A. POD; B. CAT; C. SOD; D. T-AOC; E.APX; F. MDA ) Note : Different lowercase letters a, b, c and d indicate significant differences based on p < 0.05

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The impact of cell-free filtrate of ZY-1 and FY-1 on the gene expression level of algal cells

Gene psbA1, psbD1 and rbcL code the Carboxygenase L subunits of D1, D2 and Rubp proteins which are important composite parts of PS II reaction center in the process of photosynthesis and recA codes a kind of DNA repair enzyme. Figure 5 shows that during the period of 9–72 h of ZY-1 and FY-1 cell-free filtrate treating Microcystis aeruginosa, The expression level of psbA1 was significantly higher than that of the control group, and the expression of psbD1 is close to the control group at 9 h, but is obviously lower than that of the control group during 18–72 h. The expression of rbcL is obviously lower than that of control group at 9 h, and remains a low expression within 72 h, which further indicates that cell-free filtrate can obviously affect the photosynthesis of algal cells. At 9 h of the treatment of cell-free filtrate, the expression of recA is obviously higher than that of control, but begins to rapidly decline from 18 h and the low expression maintains until 72 h. Perhaps this indicates that the cell-free filtrate of bacterial strain can activate the repair mechanism in a short time, but after more than 18 h, the cells’ self-repair ability is reduced dramatically, finally causing the cells’ lysis and death.

Fig. 5
figure 5

Effect of cell-free filtrate of ZY-1 and FY-1 on photosynthetic related gene expression in algal cell. Note : Different lowercase letters a, b, c and d indicate significant differences based on p < 0.05

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The impact of cell-free filtrate of algacidal bacteria on the rice growth under the stress of Microcystis aeruginosa

To define whether the cell-free filtrate of algaecidal bacteria can relieve the negative effect of Microcystis aeruginosa on rice, pot experiment was conducted to determine the rice seedling phenotype and its damage index treated in different ways. Figure 6 shows that the rice seedlings treated with algal liquid are short, with root dysplasia, few roots and brown roots. ZY-1 treatment group shows the number of roots has the sign of increasing, and the color of root begins to change light. FY-1 treatment group shows that the number of roots is close to that of CK1 and CK2, and the root color and plant growth are close to normal. Figure 7 shows the root scanning data, that is the root length, number of root tips, the surface area and volume of root area all lower than those of control group. All the indexes of ZY-1 and FY-1 cell-free filtrate groups are obviously increased, but slightly lower than those of the control group and the indexes of FY-1 treatment group are obviously better that those of ZY-1. So this indicates that the treatment of ZY-1 and FY-1 cell-free filtrate can relieve the damage of rice seedlings by Microcystis aeruginosa.

Fig. 6
figure 6

Growth status of rice stressed by Microcystis aeruginosa treated with cell-free filtrateof ZY-1and FY-1

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Fig. 7
figure 7

Effects of cell-free filtrate of ZY-1 and FY-1 on growth and antioxidant activity of rice seedlings poisoned by Microcystis aeruginosa.Note: Different lowercase letters a, b and c indicate significant differences based on p < 0.05

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The adversity stress of plant can be evaluated by antioxidant enzyme indicators, so we determined the content of POD, CAT, SOD and MDA in different treatment groups, further evaluated the impact of Microcystis aeruginosa on rice antioxidant system and ability to resist adversity and the effect of ZY-1 and FY-1 cell-free filtrate on relieving the damage. After treated with algal fluid, the MDA content in the roots and leaves of rice seedlings is markedly higher than CK, ZY-1 and FY-1 groups, and the activity of SOD, POD and CAT also follow the same law. The indexes of ZY-1 and FY-1 are also slightly higher than those of CK1, but FY-1 is closer to CK. Therefore, it was concluded that cell-free filtrate of the two bacterial strains can relieve the oxidative damage of rice seedlings by Microcystis aeruginosa, can restore or protect the growth of rice seedlings and the FY-1 cell-free filtrate works better than ZY-1.

Discussion

As an important player of controlling water blooms, the algae-lysing bacteria plays a significant role in the process of degrading and terminating the water blooms species [20]. According to reports, Cytophaga, Cellulophaga [21], Bacillus [22] and Pseudoalteromonas [23] all have good algae-lysing effect. Shi et al. separated the Pseudoalteromonas FDHY-MZ2 [24], and it was indicated that the bacterial strain shows strong algaecidal activity to Yumu Bennan water blooms. Chen et al.found that after 5 d of co-culture with Microcystis, clostridium Axene clone C. vulgaris can make alga dead [25]. This study screened and obtained two strains of algae-lysing bacteria–Pseudomonas helmanticensis ZY-1 and Bacillus altitudinis FY-1, when co-cultured with Microcystis aeruginosa for 7 d, the algae-lysing rate was 83.82% and 84.82% respectively. The algae-lysing experiment proved that the two bacterial strains both can lyse Microcystis aeruginosa effectively, so they can be used as the candidate strain for the control of water blooms. Amaro et al. found that the living mode of bacteria can change with the usability of nutrients and cells’ density, and these bacteria can switch from algaecidal strategy to symbiosis strategy [26]. Therefore, determining the algaecidal threshold of algae-lysing bacteria is crucial to make up an effective strategy of algae-lysing bacteria controlling algal blooms. Su et al. found that when the density of the culture medium of Raoultella R11 is higher than 3.0 × 105 cells/ml, it can split the Microcystis aeruginosa [27]; Hu found that Bacillus cereus CZBC1 has the strongest algae-lysing ability when its initial density is higher than 106 CFU/ml, and its inhibition effect will lag for 2–5 d when its density is lower than 103 CFU/ml [28]. This study found that ZY-1 and FY-1 can effectively lyse Microcystis aeruginosa densed less than 107 cells/ml when the initial bacterial density is higher than 106 CFU/ml. The algae-lysing effect on 7 d is over 80%, but the its algae-lysing ability is reduced when its bacterial density is lower than 103 CFU/ml.

At present, it was found that the algae-lysing bacteria can directly lyse alga not only by directly exposing, but in an indirect way. Bum Soo Park et al. found that HYD0802-MK36 shows a high algaecidal activity when the bacterial strains directly contacts the blue-green algae as a direct attacker [28]. Indirect lysing alga is an algae-lysing mode for most algae-lysing bacteria. Park found that the filtrate of Pseudomonas syringae KACC10292T has high-effective algae-lysing activity [29]. The study from Yu et al. shows that the activity of cell-free filtrate of HG-16 is lower after treated in high temperature, and the activity is good both treated by acid and base and is not affected by proteinase K [30]. The study from Li shows that the treatment group of washed cells of algae-lysing bacteria LY03 has higher algae-lysing rate than that of cell-free filtrate treatment group [31]. That bacterial strain lyses the chitin wrapping outside the frustule with the chitinase it releases and breaks the frustule’s cell wall, causing the death of alga. Le et al. found that β Proteobacterium genus DH15 can indirectly kill microcystis by releasing the extracellular algaecidal compound and the temperature and light both can affect its algaecidal effect [32]. This study shows the cell-free filtrate of ZY-1 and FY-1 have highly effective lysing effect on Microcystis aeruginosa. Scanning eletronic microscope shows that ZY-1 and FY-1 strains can cause the alga’s breaking and the cellular content overflowing, indicating that the two bacterial strains can kill alga in an indirect way through secreting some active substance and when the substance is 25–75℃ and pH is within 5–9, the strains have obvious algae-lysing effect.

Zhang et al. found that tripyrrole ring-Prodigiosin produced by Hahella sp.KA22 can indirectly lyse Microcystis aeruginosa [33]. Prodigiosin goes through the membrane by specific ABC transporter protein, and then can induce lipid peroxidation by stimulating the excessive production of active oxygen in algal cells and cause oxidative damage of the algal membrane system, and further leading to dysfunction of the photosynthetic system and finally causing the death and split of Microcystis aeruginosa [33]. As important parameters that reflect the photosynthetic efficiency of algal cells, Fv/Fm, ΦE0, PiAbs, Ψ0 are closely related to the photosynthetic electron transport rate and the degree of light loss in photosynthetic systems. Hou et al. exposed the Microcystis aeruginosa to the filtrate of Bacillus altitudinis G3 and found that Fv/Fm and PiAbs of the filtrate group were lowering continuously, and obviously lower than that of control group after 0 h, indicating that G3 filtrate significantly inhibit the photosynthetic efficiency of Microcystis aeruginosa [34]. This study found that when ZY-1 and FY-1 cell-free filtrate was used to treat the alga, the Fv/Fm, ΦE0, PiAbs and Ψ0 of alga are in the downward trend, indicating that the photosynthetic electron transport rate at that time is slow and the photosynthetic system of alga is suppressed. PSII system is sensitive to the adverse environment [35]. The light intensity, temperature and biological stress can lower Fv/Fm [36], further inhibiting phtotsynthesis. RT-qPCR shows that in the process of cell-free filtrate treating algal cells, the expression level of the important composite protein genes in the reaction center of alga PSII--psbD1, psbA1 and the Rubp carboxygenase gene rbcL in the photosynthetic process are all lowered, indicating that ZY-1 and FY-1 cell-free filtrate can not only break or inhibit the photosynthetic system of alga, but can suppress the expression of the key coding gene and protein in the photosynthetic system.The cell-free filtrates of ZY-1 and FY-1 had an effect on the photosynthesis of algal cells and attacked the photosystem II of algal cells, on the 7th day, Fv/Fm of Microcystis aeruginosa decreased by 97.22% compared with the control group. In addition, this study also found RecA gene that codes DNA repair enzyme has a higher expression on 9 h than that of CK, but from 18 h it begins to lower. This suggests that after a short-term treatment by cell-free filtrate, algal cells remain some repair ability, but a long-term treatment can make the algal cells completely lose the repair ability. In this study, antioxidant enzyme system and DNA content also further prove this inference. The SOD, POD and CAT of algal cells treated by ZY-1 and FY-1 cell-free filtrate all show the tendency of increasing first and decreasing afterwards and MDA is increasing continuously, and the cell-free filtrates of ZY-1 and FY-1 had an effect on the MDA content increased to 0.49 ± 0.01 nmol protein and 0.48 ± 0.02 nmol protein respectively, which indicates that cell-free filtrate can have effect on algal cells for a long term and make the cells’ degree of oxidative damage increasing until dead. This comes to conclusion, the algaecidal process of ZY-1 and FY-1 may be that cell-free filtrate inhibits the photosynthesis of Microcystis aeruginosa and at the same time avoid the alga’s photosynthesis renewing and restoring, through affecting the gene expression level and breaking the repair system of algal cells. So that causes exacerbating membrane lipid peroxidation, and the breaking of algal membrane, which makes the cells not able to do normal living activities, realizing the goal of highly-effectively kill algal cells.

MCs released by Microcystis aeruginosa and other toxic metabolites can transfer into the farmland through irrigation, causing adverse effect on the growth and production of rice and other plants. Chen states that high-density MC-LR inhibits the elongation of primary roots in rice, the formation of crown root and the development of lateral root, and also hinders the morphogenesis of rice’s roots [37]. This study also found that Microcystis aeruginosa affects the rice growth in seedling period, and the roots and the aboveground parts are all obviously damaged, so the roots develop slow and have the sign of turning brown. And MDA content, and the activity of SOD, POD and CAT of the rice seedlings also prove this point. The addition of Microcystis aeruginosa decreased the number of root tips by 43.23% compared with CK, the root length, root diameter, root volume, root surface area and root projection area also decreased, and the MDA content of rice increased to 1.02 µmol/g. The content of MDA decreased to 0.9 ± 0.09 µmol/g and 0.94 ± 0.05 µmol/g, respectively, and the activities of SOD, POD and CAT decreased significantly after administration of ZY-1 and FY-1 cell-free filtrate, reduced Microcystis aeruginosa damage to rice seedlings.After treated by ZY-1 and FY-1 cell-free filtrate, the degree of oxidative damage to the rice roots is obviously lowered, relieving the harm caused by Microcystis aeruginosa and having some effect of restoring the roots and aboveground parts of rice seedlings. And FY-1 cell-free filtrate has better effect than ZY-1. Therefore, for the two bacterial strains of ZY-1 and FY-1 have indirect algaecidal traits, they can be used as candidate algae-lysing bacterial strain of environmentally-friendly and have a broad application in agricultural production and the control of water blooms.

Conclusion

Pseudomonas ZY-1 and Bacillus FY-1 indirectly dissolve Microcystis aeruginosa. The cell-free filtrate of the strain affects the photosynthesis of algae cells, attacking the photosystem II of algae cells, which resulted in impaired photosynthesis, decreased fv/fm and down-regulated expression of psbA1, psbD1 and rbcL genes. Meanwhile, the cell-free filtrates of ZY-1 and FY-1 increased the content of MDA in Microcystis aeruginosa, which resulted in oxidative damage to the algal cells, activated the antioxidant enzyme system of the algal cells, and increased the secretion of SOD, POD, CAT, APX and T-AOC. Microcystis aeruginosa can cause peroxidation damage to the roots of rice, leading to a decrease in root tip number, root length, root diameter, root volume, root surface area, root projection area, and other indicators during the seedling stage. The application of cell-free filtrates of ZY-1 and FY-1 significantly reduced the MDA content in the roots and leaves of rice seedlings, as well as the activity of antioxidant enzymes such as SOD, POD, and CAT, alleviating the harm of Microcystis aeruginosa to rice seedlings.

In this study, the algae-lysing properties and mechanisms of ZY-1 and FY-1 on Microcystis aeruginosa were studied, and their effects on algal blooms were studied on a small scale in hydroponic rice. The study provides some theoretical basis and application value for biological control of harmful algal blooms.

Data availability

Sequence data that support the findings of this study have been deposited in (National Center for Biotechnology Information with the primary accession number(s) can be found at: https://www.ncbi.nlm.nih.gov,code PP214940; https://www.ncbi.nlm.nih.gov, PP214911.

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Acknowledgements

Thank you to Jilin Province soybean regional technology innovation center for providing certain experimental equipment and an experimental site for our research. Thanks to Shenzhen Oudebao Translation Co., Ltd. for the language help.

Funding

This study was supported and funded by the Science and Technology Development Plan Project of Jilin Province (20240101234JC) .

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  1. College of Life Science, Jilin Agricultural University, Changchun, Jilin, China

    Lei Wu, Xueying Zhou, Yuan Zhu, Jianing Wang, Chengcai Yue, Yufeng Xu, Shiqi Tian, Siyuan Li, Xue Yang & Meiying Yang

  2. Faculty of Agronomy, Jilin Agricultural University, Changchun, Jilin, China

    Xiaoshuang Wei & Zhihai Wu

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Contributions

L.W., X.Z., Y. Z., M. Y. and X.Y completed the screening and identification of algicidal bacteria. L.W., J.W., C. Y., X.Y. and M. Y. were responsible for the research on the algicidal mechanism of strain ZY-1 and FY-1. Y. X., S.T., S. L., X.W. and Z. W. conducted a pot experiment on rice. L.W. interpreted the data and wrote the manuscript with input from all co-authors. All authors contributed to the article and approved the submitted version.

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Wu, L., Zhou, X., Zhu, Y. et al. Pseudomonas ZY-1 and Bacillus FY-1 protecting the rice seedlings from the harm of Pseudomonas aeruginosa via indirect seawead lysis. BMC Microbiol 24, 375 (2024). https://doi.org/10.1186/s12866-024-03509-9

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