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The Role of Gamma Irradiation on Growth and Some Metabolic Activities of Spirulina platensis ( 99 )

ABSTRACT

KEYWORDS

The Role of Gamma Irradiation on Growth and Some Metabolic Activities of Spirulina platensis.

Moussa, H.R1; Ismaiel, M.M.S.2; Shabana, E.F.3; Gabr, M.A.3 and El-Shaer, E.A.1

Received: 02/03/2015

Accepted: 06/04/2015

Available on line: 30/06/2015

E.mail:[email protected]

Gamma Irradiation, Pigments, Photosynthetic Activity, Spirulina Platensis, Carbohydrates, Carboxylating Enzymes.

J. Nucl. Tech. Appl. Sci, Vol. 3, No. 2, PP. 99 : 107 (2015)

Journal of

NUCLEARTechnology in Applied ScienceISSN 2314-8209 e-ISSN 2314-8217

1. Radioisotope Department, Nuclear Research Centre, Atomic Energy Authority.2. Faculty of Science, Zagazig University.3. Faculty of Science, Cairo University.

Spirulina platensis cells were exposed to different doses of gamma irradiation 0.0; (control), 0.5, 1.0, 1.5, 2.0, 2.5 and 3.0 Kilo Gray (kGy) using Co60 as a gamma source at the Cyclotron Unit, Nuclear Research Center, Egyptian Atomic Energy Authority. After which, the cells were cultivated on Zarrouk medium for 14 days (the exponential phase of growth). The optimum growth of Spirulina platensis was recorded at 2.0 kGy as compared to the control after the 14th day of incubation. All of the following analyses were done after 10 days of growth. The results of pigments analysis revealed that the chlorophyll a and carotenoid con-tents of Spirulina platensis were reached their maximum rate at a dose of 2.0 kGy, Which induces the same trend for phycobiliprotein fractions. The photosynthetic activity and total carbohydrate content of the irradi-ated Spirulina cells increased with elevating the doses of gamma irradia-tion and reached a maximum value at a dose of 2.0 kGy as compared to the control. The activity of ribulose-1,5-bisphosphate-carboxylase/oxygenase (RUBISCO) was increased up to irradiation dose of 2.0 kGy. whereas, the maximum activity of the phosphoenol pyruvate carboxylase (PEPCASE) was recorded at the irradiation dose of 1.0 kGy.

INTRODUCTION

The cyanbacterium Spirulina is an ideal nutritional supple-ment and can be the answer to malnutrition problems in developing countries (Vendan and Rajeshwari, 1998). Spirulina contains remarkable concentrations of nutrient elements, thereby making it as a whole food alternative to isolated vitamins and minerals (Venkataraman, 1989).

Moussa, H.R.( 100 ) J. Nucl. Tech. Appl. Sci., Vol. 3, No. 2

The numerous therapeutic and health-improving properties of Spirulina are truly amazing, as it is rich in vitamins, minerals, and antioxidants, all of which make it highly beneficial as an anti-aging, anti-can-cer, and super-detoxifying marvel food (Moorhead et al., 2011). Spirulina is one of the most promising micro algae as well as micro algal biotechnology be-cause it is easy to grow and having a simple harvest and drying process (Kumar et al., 2011). Spirulina platensis has tremendous importance in nutritional, industrial and environmental biotechnology (Lodi et al., 2003), it is considered as an excellent food, lack-ing toxicity and having corrective properties against viral attacks, anemia, tumor growth and malnutri-tion (Campanella et al., 1999). Many pigments like carotenoids, chlorophyll “a” and phycocyanin are present in Spirulina, considered too important anti-oxidants and are responsible for many characteristic colors (Singh et al., 2014). On the other hand spi-rulina can actually help in weight loss, increasing friendly micro flora in the intestines and improve di-gestion (Moorhead et al., 2011). The high content of protein in Spirulina indicates relatively good amino acid profile enabled the use of algal biomass as feed supplement (Gaese, 2012). Spirulina platensis con-tains about 13.6% carbohydrates as dry weight; some of these are glucose, rhamnose, xylose, mannose and galactose (Shekharam et al., 1987). Gamma rays have been proved to have economical and effective uses as compared to other ionizing radiations be-cause of its easy availability and the power of pen-etration (Moussa, 2006). This penetration power of gamma rays has a wide application in improvement of various plant species (Moussa, 2006), and stimu-lated growth of Spirulina platensis (Weidang et al., 2008). Gamma radiation can be useful for alteration the physiological characters (Ali et al., 2008), and may increase the enzymatic activity and stimulat-ing the rate of cell division (Heidarieh et al., 2012). Gamma rays could enhance the growth of Spirulina platensis (Tianci et al., 1990).

The goal of this work is to evaluate the effect of gamma radiation (estimation the optimum dose)

for increasing the nutritional and commercial value of Spirulina platensis via stimulating the pigments, photosynthetic activity, total carbohydrates content and growth.

MATERIALS AND METHODS

Spirulina platensis was obtained from the Phy-cology Lab, Faculty of Science, Zagazig University, Egypt. Spirulina was grown in batch cultures in Zar-rouk medium (Zarrouk, 1966). To 500 mL Erlen-meyer flasks, a 250 mL of Zarrouk medium were added and autoclaved at 1.5 atmp for 20 minutes. After cooling, the flasks were inoculated with equal inoculums of Spirulina. Incubation was carried out in the growth chamber at the Radioisotope Depart-ment, Nuclear Research Center, Atomic Energy Au-thority, at 31±1°C and illuminated by white fluores-cent lamps at light intensity (60µmol photons m-2s-1).

The cultures were hand shaked once daily and were sub cultured every two weeks to ensure a regu-lar supply of exponentially growing algal cells. The flasks were exposed to different doses of gamma irradiation; 0.0, 0.5, 1.0, 1.5, 2.0, 2.5 and 3.0 kGy using Co60 as gamma source at the cyclotron unit, Nuclear Research Center, Egyptian Atomic Energy Authority.

A complete death for the organism was occurred at the dose of 3.0 kGy. Three replicates for each treatment in a randomized design and all biochemi-cal analyses were done during the exponential phase of growth (10 days). Growth was measured as opti-cal density by monitoring change in absorbance at wave length 560 nm by means of spectrophotometer (UNICAM UV-Visible spectrometer, Helios, United Kingdom) according to Wetherell (1961).

The quantitative estimation of chlorophyll “a” and carotenoids was determined as described by APHA (1985). Estimation of phycobiliprotein frac-tions; c-phycocyanin, allophycocyanin, phycoery-thrin and total phycobiliprotein, was carried out ac-cording to Lamela and Márquez-Rocha (2000).


Determination of total carbohydrates was done as described by Dubois et al. (1956). Phosphoenol py-ruvate carboxylase assay (PEPCASE, EC 4.1.1.31) was measured using the method adopted by Cánovas and Kornberg (1969). Ribulose-1,5-bisphosphate-carboxylase/oxygenase (RUBISCO, EC 4.1.1.39) activity was measured using the method given by Robinson and portis (1988). Photosynthetic activ-ity (14CO2-assimilation) was assayed according to Moussa (2006).

RESULTS

Spirulina platensis was irradiated with differ-ent doses of gamma irradiation in addition to con-trol, then the growth was followed by measuring the optical density at 560 nm two days interval for two weeks. Figure (1) showed gradual increase in growth value at most concentrations with lapse of time to reach maximum at the 14th day of growth. It was observed that the growth of Spirulina was increased significantly (p≤0.05) with increase in time at lower and moderate gamma ray doses. The growth at the 14th day when irradiated by 0.5, 1.0, 1.5 and 2.0 kGy increased significantly (p≤0.05) by percentages of 3%, 15%, 23% and 32%, respectively in compari-son with control. On contrary, by increasing the dose to 2.5 kGy, a significant (p≤0.05) decrease in the growth occurred by (35%) at the 14th day when com-pared to control. Two way ANOVA analysis showed that different doses of gamma irradiation affect sig-nificantly (p≤0.05) the growth of S. platensis and the maximum growth was occurred at 2.0 kGy.

The results of pigment analyses in Figure (2) re-vealed that chlorophyll «a” and carotenoid contents of Spirulina platensis were significantly (p≤0.05) in-creased with increasing the doses of gamma irradia-tion up to 2.0 kGy. A significant (p≤0.05) increase of chlorophyll “a” occurred at the dose 1.5 kGy (30%) where, the maximum increase occurred at 2.0 kGy (48%). However, carotenoids content, recordes a significant (p≤0.05) stimulation at a dose of 1.5 and 2.0 kGy by 100% and 129% respectively when compared to control. On the other hand, there was an inhibitory effect of gamma irradiation at 2.5 kGy in both chlorophyll «a” and carotenoids in a signifi-cant (p≤0.05) difference as compared to the control but the reduction in chlorophyll “a” (43%) was more significant (p≤0.05) than those of carotenoids (22%) as compared to the control. One way ANOVA analy-sis showed that different doses of gamma irradiation affect significantly (p≤0.05) the chlorophyll «a» and carotenoid levels of Spirulina, the maximum stimu-latory dose for both was 2.0 kGy and the inhibitory dose was 2.5 kGy.

Results of Figure (3) revealed that gradual and significant (p≤0.05) increase with some minor fluc-tuations occurred in phycobiliprotein fractions of S. platensis by increasing the gamma irradiation dose to reach maximum at 2.5 kGy by 148%, 22%, 175% and 63% for phycocyanin, allophycocyanin, phy-coerythrin and total phycobiliprotein, respectively. However, allophycocyanin content was the high-est fraction of phycobiliprotein in Spirulina either in treated or untreated samples. One way ANOVA analysis showed that different doses of gamma ir-radiation affect significantly (p


Data shown in Table (1) revealed that total car-bohydrates content reflected significant (p≤0.05) and gradual increase up to 2.0 kGy, which increased by

84% as compared to control. While, a significant (p≤0.05) decrease than the control sample observed at the dose of 2.5 kGy with a percentage of 54%.

On the other hand, the photosynthetic activity of Spirulina also increased with increasing the radia-tion dose and there is a significant (p≤0.05) differ-ences between the different treatments. Maximum photosynthetic activity was observed at 2.0 kGy and it was increased by 199% as compared to the con-trol. On contrary to carbohydrates, the dose 2.5 kGy stimulated the photosynthetic activity by 72% . One way ANOVA analysis showed that different doses of gamma irradiation affected significantly (p≤0.05) to-tal carbohydrates content and photosynthetic activity of S. platensis.

Means marked with the same superscript letters are not-significant (p≥0.05), whereas others with different superscript letters are significant (p≤0.05). Data represented the mean ± SD.

Results of Figure (4) indicated that the activity of ribulose 1,5 bisphosphate carboxylase/oxygenase in S. platensis increased significantly (p≤0.05) at a dose of 2.0 kGy by 87% as compared to control. But, when radiation dose was increased to 2.5 kGy there was a significant (p≤0.05) decrease was observed but it still more than values of untreated samples with percentage increase (45%). Results showed also

that the activity of phosphoenol pyruvate carboxyl-ase increased gradually and significantly (p≤0.05) till the dose of 1.0 kGy, order of the increase was (40% and 55%) for 0.5 and 1.0 kGy, respectively. However there was a significant (p≤0.05) decrease occurred by 24% and 33% at the dose of 2.0 and 2.5 kGy respectively when compared to untreated sam-ples. One way ANOVA analysis showed that differ-ent doses of gamma irradiation affected significantly (p≤0.05) the activity of Ribulose 1,5 bisphosphate carboxylase/oxygenase and phosphoenol pyruvate carboxylase enzymes.

0 0.5 1 1.5 2 2.5

Fig.(3): Phycobiliproteins of S. platensis exposed to dif-ferent doses of gamma irradiation after10 days of growth. Vertical bars represent means ± SD.

Table (1) Effect of different doses of gamma irradiation on total carbohydrates content and photosynthetic activity of Spirulina Platensis after 10 days of growth.

Gamma irradiation dose(kGy)

Total carbohydrate contents(mg glucose/g Dwt)

photosynthetic activity (KPq /mg Fwt)

0.0 216±64.5b 7.80±0.75a

0.5 246±31.0bc 9.30±0.56b

1.0 305±7.10cd 11.1±0.70c

1.5 352±32.2d 14.9±0.65e

2.0 397±61.7e 23.3±0.75f

2.5 100 ±31.9a 13.4±0.55d


DISCUSSION

Spirulina platensis has been known to be wide-ly distributed at all environments. This distribution may lead to subjection to many types of harmful stresses including salinity, heavy metals and irradia-tion (Sharma et al., 2012 and Cheng et al., 2013)

Gamma rays have been proved to have econom-ical and effective uses compared to other ionizing radiations because of its easy availability and the power of penetration (Moussa, 2006). The aim of this work was to evaluate the commercial and eco-nomical production of Spirulina platensis treated with different doses of gamma irradiation.

In the present work, the growth of S. platensis was affected by the concentration of the applied ir-radiation doses. The algal cells showed an enhance-

ment towards the relatively low to moderate dose concentrations (up to 2.0 kGy) then this growth de-clined at 2.5 kGy these results were confirmed by Weidang et al.(2008) who irradiated S. Platensis by different doses of gamma irradiation (from 0.0 to 3.0 kGy) and recorded that the best growth was at 1.5 kGy and the LD50 was at 2.0 kGy they also record-ed that even 3.0 kGy didn’t cause complete death to Spirulina and mentioned that Spirulina has stronger ionization radiation proof and self-rehabilitation ca-pacity. On the other side, Chlorella pyrenoidosa mu-tants that resulted from the irradiation at 300 and 500 Gy grew better than the original strain (control) and the same with Chlorella. vulgaris irradiated at 500 Gy, however, high doses of gamm rays caused cell damage or even death (Cheng et al., 2013). Also, low dose of Gamma rays (less than 1.0 kGy) could stimulate the growth of Spirulina platensis. (Tianci et al., 1990). Gamma irradiation was reported to induce oxidative stress with overproduction of re-active oxygen species such as superoxide radicals, hydroxyl radicals, and hydrogen peroxides, which react rapidly with almost all structural and function-al organic molecules including proteins, lipids, and nucleic acids causing disturbance of cellular metabo-lism (Al-Rumaih & Al-Rumaih, 2008). Unless the concentrations of these free radicals are controlled by antioxidants, they may damage proteins, DNA, lipids and other molecules (Halliwell and Gutter-idge, 1989).

Therefore, S. platensis cells were found to stim-ulate several antioxidant systems to control the ROS generation and levels. For instance, the increased production of carotenoids content and chlorophyll “a” along with the increased concentration of irra-diation doses Our results showed that the optimum values of chlorophyll “a” and carotenoid contents were recorded at 2.0 kGy and declined at 2.5 kGy. In comparing with control, this can be explained as a potent strategy to relief the harmful effect of gamma irradiation. Carotenoids were known to be the most important antioxidants against the ROS. They are not only help in the photosynthetic process but also pro-tecting the light-harvesting pigments in the antenna complexes against photochemical damage caused

Fig.(4): Effect of different doses of gamma irradiation on ribulose 1, 5 bisphosphate carboxylase and phosphoenol pyruvate carboxylase activity of Spirulina platensis after 10 days of growth.

0 0.5 1 1.5 2 2.5

0 0.5 1 1.5 2 2.5


(for example) by ROS (Woodall et al., 1997). On the other hand, the studies of Ben-Amotz et al. (1989) reported the role of carotenoids as antioxidants such as β-carotene and astaxanthin in protecting algae against the damage caused by high irradiance

The tolerance of the algal cells to the gamma radiation by increasing carotenoids may enhance growth and other cellular components such as chlo-rophyll “a”. Abu et al.(2005) reported the increased pigment contents (chlorophyll a, b) in Paulownia tomentosa plants after exposure to gamma radiation (20 Gy). Moreover, they elucidated that the conse-quence increase of photosynthesis was due to the improvements in the leaf water balance. El-Beltagi et al. (2013) recorded increments of chlorophyll a, b, carotenoids and total photosynthetic pigment con-tents in leaves of cowpea plants after treatment with gamma radiation (50 Gy). However, the higher doses may have a lethal effect on pigments content. Anoth-er support by the workers Agarwal et al.(2008), and Borzouei et al. (2010) who claimed that chlorophyll a, b and total chlorophyll levels in Triticum aestivum increased by 64.5% after exposing to 100 and 200 Gy of gamma rays when compared to non-irradiated treatments.

Also, the results revealed that the optimum val-ues of phycobiliproteins were recorded at 2.5 kGy, Figure (3). Cano-Europa et al. (2010) suggested that phycobiliproteins are powerful antioxidants that prevent oxidative stress because of their nucleophilic ability to neutralize reactive oxidants (ROS). In this regard, Kumar et al. (2011) reported that the accu-mulation of phycobiliproteins may be an acclamato-ry mechanism for the red alga Gracilaria corticata in response to salinity induced stress Phycobiliproteins composed of more than 60% of the total soluble pro-tein of the algal cells (Bennett and Bogorad, 1971). Also, Weidang et al.(2008) proved that low dose of gamma rays, less than 1.5 kGy, could improve the content of phycobilin of Spirulina.

Findings of total carbohydrates and photosyn-thetic activity revealed that gamma irradiation can influence photosynthesis of S. platensis cells and stimulates the 14CO2 fixation rate of the cell, thereby

improve algal growth (Agarwal et al., 2008). The enhancement of photosynthetic activity may be ex-plained on the basis of the increased pigments, ca-rotenoids and phycobiliprotein contents of the irra-diated S. platensis cells. However, Luckey (2008) showed that continuous irradiation of the photosyn-thetic bacterium, Rhodopseudomonas capsulata, and the blue-green alga, Anacystis nidulans with gamma rays, without light, increased the photosynthesis of the two photosynthetic organisms.

Low doses of gamma rays highly significantly increased the level of carbohydrate constituents (Nouri and Toofanian, 2001 and Moussa, 2011). Also, Khodary and Moussa (2003) reported that treatment of dry seeds of lupine with gamma rays at (20 Gy) increased the total chlorophyll content, soluble sugars and photosynthetic activity.

The enhancement of the activities of the carbox-ylating enzymes at low doses of gamma radiation may reflect the efficiency of photosynthetic process and/or the carbon dioxide fixation under the rela-tively low irradiation doses (Agarwal et al., 2008). However, Moussa (2011) reported that the relatively low dose of gamma radiation (20 Gy) could stimu-late the activities of phosphoenol pyruvate carbox-ylase and ribulose-1,5-bisphosphate carboxylase / oxygenase of drought-stressed soybean plants. In addition, the increase in PEPCASE activity may further increase RUBISCO activity by anaplerotic C flow (i.e. malate), and may promote starch synthesis (Zhang et al., 2012).

CONCLUSION

This study focused on evaluating of the effect of gamma irradiation on some metabolic activities of spirulina (carbohydrates, photosynthetic activ-ity, some carboxylating enzymes, chlorophyll a and carotenoids) and the cell growth that could lead to increase in economical and commercial value of this blue-green alga. The current results provide some evidences to increment of certain cellular compo-nents such as pigments, carbohydrate, and enzymes. On the other hand, gamma irradiation with relatively


higher doses of gamma rays (≥2.5 kGy) decreased the cellular activities and ultimately resulted in the death of cells.

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دور التشعيع اجلامى يف النمو وبعض العمليات األيضية لطحلب إسبريولينا بالتينسيس

هالل رجب موسى1 ، مصطفى حممود سامي إمساعيل2 ، عفت فهمي شبانه3 ، حممود على جرب 3 ، ايناس على الشاعر1

من املعروف أن طحلب إسبريولينا بالتينسيس هو طحلب غنى بالربوتينات والفيتامينات واملعادن وقد أثبتت الدراسات قدرته الفائقة على مقاومة الكثري من األمراض مثل االيدز وفريوس سى وبعض األورام

السرطانية ومن هذا املنطلق فقد اهتمت الدراسة بهذا الطحلب

استهدفت هذه الدراسة تقييم مدى تأثري اإلشعاع اجلامى على منو وبعض األنشطة األيضية لطحلب العلوم النبات كلية إسبريولينا بالتينسيس ومن أجل حتقيق هذه األهداف مت جلب الطحلب من قسم جامعة الزقازيق وزراعته يف البيئة املخصصة لنموه ثم مت تشعيع الطحلب جبرعات خمتلفة بدأت من (kGy 2.5 .2.0 .1.5 .1.0 .0.5 .0.0) ثم متت الزراعة مرة أخرى حتت ظروف حمكمة ومت أجراء التحاليل أثناء

الطور اللوغاريثمى بعد عشرة أيام من النمو.

وقد تبني إن النمو قد ازداد تدرجييا حتى وصل إىل أفضل منو عند 2 كيلو جراى باملقارنة بالذي مل بالتناقص عند ازدادت ثم بدأت الكلوروفيل والكاروتني قد البناء الضوئي مثل يتم تشعيعه وأيضا أصباغ زيادة اجلرعة إىل 2.5 كيلو جراى ومن ناحية أخرى فان عملية البناء الضوئي واإلنزميات املصاحبة هلا بل وأيضا الكربوهيدرات الكلية ناتج البناء الضوئي قد ازدادت أيضا باملقارنة الذي مل يتم تشعيعه مسجلة

أعلى قراءات عند جرعة 2 كيلو جراىاملستخدمة وأن انه توجد اختالفات معنوية بني كل اجلرعات التحاليل اإلحصائية على وقد دلت

أفضل جرعة قد حققت أفضل منو للطحلب هي 2.0 كيلو جراى.

)2015( ، 107 : جملد 3 ، عدد 2 ، ص 99

مجــــلة

التقنيــات النــوويــة فى العلوم التطبيقية

يصدرها

اجلمعية امل�شرية للعلوم الإ�شعاعية وتطبيقاتها

املوقع اإللكتروني www.esrsa.com

البريد اإللكتروني [email protected]

مجـــــــــلد 1

عدد 1 (2013)

قسم النظائر املشعة - مركز البحوث النووية - هيئة الطاقة الذرية.. 1قسم النبات - كلية العلوم - جامعة الزقازيق.. 2قسم النبات - كلية العلوم - جامعة القاهرة.. 3

spirulina platensis.esrsaeg.net/2 new book 99-108.pdf · spirulina platensis cells were exposed to...

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