Biological activities of derived pigments and polyphenols from newly recorded alga; Phyllymenia gibbesii

doi:10.21203/rs.3.rs-3899585/v1

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Biological activities of derived pigments and polyphenols from newly recorded alga; Phyllymenia gibbesii

https://doi.org/10.21203/rs.3.rs-3899585/v1

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published 11 Sep, 2024

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The newly recorded Phyllymenia gibesii in the Mediterranean Sea at Alexandria coast of Egypt is regarded a significant source of bioactive substances and applied as an antioxidant, anti-inflammatory, and antimicrobial agents. According to the HPLC chromatograms, the acetone extract of P. gibesii comprised ten photosynthetic pigments (chlorophyll-a, chlorophyll-d, α-carotene, β-carotene, phycocyanin, allophycocyanin, antheraxanthin, β-cryptoxanthin, lutein, and violaxanthin). Total carotenoids were the dominant class in the pigments' profile, achieving a concentration of 257 g/g. The P. gibbesii extract had a total content of phenols as; 146.67 mg/g and a total content of flavonoid as; 104.40 mg/g. The capacity of all the investigated biological activities augmented with the concentration of the algal extract. The maximal DPPH scavenging capacity was 81.44%, with an inhibitory concentration value (IC50); 9.88 μg/mL. Additionally, the highest ABTS scavenging capacity was 89.62%, recording an IC50 value of 21.77 μg/mL. The hemolytic activity of P. gibbesii attained a maximum capacity of 49.88%, exhibiting an IC50 value of 100.25 μg/mL. Data also showed the maximum anti-inflammatory effectiveness as; 81.25%, with an IC50 value of 99.75 μg/mL. Furthermore, the extract exhibited antimicrobial capacity against all reference strains, particularly at high concentration (0.1 mg/mL). The extract had the greatest effect on C. albicans and E. coli.

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Marine macroalgae comprised three groups, among which the Rhodophyceae (red algae) are the most diversified over the world (circa 6131 species)¹. Numerous types of red algae serve as a good source of natural substances with significant biological functions involving antimicrobial², antihyperlipidemic³,antidiabetic⁴ antitumors⁵, anti-inflammatory⁶, and antioxidant activities⁷.

The benefits to human health are taken into account when using red algae antioxidants in foods, food supplements, nutraceuticals, and medicines ⁸. Red algae have gained significant economic value from these bioproducts, such as agar and carrageenan, making them a valuable commodity from an industrial view⁹. However, the concentration and composition of bioactive substances in seaweeds might vary across individuals, depending on their environment, the season, and other factors. Regarding climatic change, the environmental factors affecting intertidal algae are contentiously changing. To deal with shifting of environmental conditions, seaweeds involving red algae had modified specific adaptive metabolic responses, making them able to withstand and adapt to various abiotic pressures¹⁰.

Furthermore, pigments of red algae showed a diverse spectrum of biological functions. As photoautotrophic, they own chlorophyll-a and chlorophyll-d and accessory pigments which are particular to this group¹¹. According to their chemical structure, pigments of red algae have been broadly grouped into main categories as follows: closed tetrapyrroles (such as chlorophyll-a and chlorophyll-d), open tetrapyrrols (e.g., phycobilipigments), and carotenoids (e.g., polyisoprenoids)¹¹. Because of their significant biotechnological potential, they have been used in numerous commercial applications and registered patents. These pigments also exist in many colors and have been effectively used throughout history in daily life. A few instances worth mentioning include food, paper and textile industries, water technology, and agricultural practice¹². Interestingly, pigments exhibit advantageous biological activity as antioxidants and anticancer agents, as well as several key features, which make them suitable in these various industrial contexts¹². Therefore, they have a significant potential of meeting current market needs, which increasingly focus on the health and biotechnology sectors in search for natural substances having positive effects on the health of human¹³. However, there are still issues with optimizing and then scaling up extraction and purification processes, particularly when taking into account the needs for both quantity and quality from an industrial and commercial perspective¹⁴.

In particular, the red alga Grateloupia gibbesii was newly introduced in the Egyptian coast of Mediterranean Sea¹⁵. Currently, this species has been identified as a synonym of Phyllymenia gibbesii¹⁶. Many studies are focused on the aliens species in the Mediterranean Sea, which cause many impacts on the introducing area such as change in biodiversity, competition between these alien species and native ones¹⁷. In addition, some of them have the potential to be detrimental to the ecosystem and to other macroalgal species. Thus, it would be of interest to find out valuable substances in the domain of health and nutrition from biomass of alien species in order to compensate for expense of the eradication and as a safe and eco-friendly solution to the problem of the introduction¹⁸.

The basic target of the current study is investigating several biological activities of different pigments detected in the newly recorded alga Phyllymenia gibbesii and to assess the concentration of these pigments.

Macroalgae are significant basis for the therapeutically valuable compounds. They are regarded as a source of unique types of biologically active substances used in several domains due to their diversity and chemical differences. Herein, the antioxidant, anti-inflammatory, hemolytic, and antibacterial properties of P. gibbesii acetone extract was evaluated. Its pigments were also examined to further clarify the chemical constituents.

HPLC chromatographic analysis. To identify pigments bioactive compounds in P. gibbesii acetone extract, HPLC has been used. The P. gibesii chromatograms showed10 individual photosynthetic pigments: chlorophyll-a, chlorophyll-d, phycocyanin, allophycocyanin, α-carotene and β-carotene, antheraxanthin, β-cryptoxanthin, lutein, and violaxanthin (Fig. 1–7). The two pigments; phycoerythrin and zeaxanthin, were not detected by the HPLC. The chromatogram showed that chlorophyll-d was one of the characteristic chlorophylls of P. gibbesii, with lower concentration of 25.95 µg/g than that of chlorophyll-a (41.65 µg/g) (Table 1). Among the phycobiliproteins (PBP), the allophycocyanin (APC) was the dominant pigment (41.95 µg/g), while the phycocyanin (PC) attained only the half of APC (20.60 µg/g) (Table 1).

Table 1

Pigments content of *P. gibbesii* acetone extract (µg/g) analyzed by chromatographic HPLC.
Pigments	Pigments concentration (µg/g)
Chlorophylls
Chlorophyll-a	41.65
Chlorophyll-d	25.95
Total chlorophylls	67.60
Phycobiliproteins
Phycocyanin	20.60
Phycoerythrin	Not detected
Allophycocyanin	41.95
Total phycobiliproteins	62.55
Carotenoids
Carotenes
α-Carotene	76.10
β-Carotene	80.60
Total carotenes	156.70
Xanthophylls
Antheraxanthin	19.00
β –cryptoxanthin	42.50
Lutein	31.30
Violaxanthin	7.50
Zeaxanthin	Not detected
Total xanthophylls	100.30
Total carotenoids	257.00

The carotenes were the most representative pigments in the carotenoids class. The concentration of β-carotene (80.60 µg/g) was comparable to α-carotene (76.10 µg/g). Their total concentration (156.70 µg/g) exceeded that of the total chlorophylls (67.60 µg/g) and total phycobiliproteins (62.55 µg/g) (Table 1). Concerning the xanthophylls, the second group in the carotenoids, it was represented by four pigments; antheraxanthin, β-cryptoxanthin, lutein and violaxanthin, with concentration of 19.00, 42.50, 31.30, and 7.50 µg/g, respectively. However, the total carotenoids were the dominant class in the pigments' profile attaining a concentration of 257 µg/g (Table 1).

Because of a substance known as sodium-copper-chlorophyllin, chlorophyll has anti-cancer and antioxidant properties. Supplementation with chlorophyllin before meals has been proven to diminish the harm caused by aflatoxin, a highly carcinogenic mold that grows on some foods¹⁹. In high-risk populations, the usage of chlorophyllin may aid in the prevention of liver cancer caused by aflatoxin. Moreover, the chlorophyll metabolites like phytanic acid can be used to treat and prevent diabetes²⁰. Phytanic acid has also an effect on the expression of genes related to glucose metabolism via different natural peroxisome proliferator-activated receptor isoforms²¹.

According to Dasgupta²², chlorophyll-a and chlorophyll-d are two of the pigments of red algae. In contrast, Kato and his co-workers²³ mentioned that red seaweeds have only chlorophyll-a. However, the detection of chlorophyll-d is dependent on the choice of solvent for extraction process²⁴. In this trend, Osório and his co-workers²⁵ investigated the red alga Porphyra sp. for pigment content using a variety of solvents. Their findings indicated that acetone was the most suitable solvent for detection of chlorophyll-d, resulting in a maximum of 16.25 µg/g, while it was absent using N-dimethyl formamide solvent. In the present study, using acetone as solvent gave the opportunity to determine chlorophyll-d in P. gibbesii (25.95 µg/g) and chlorophyll-a (41.65 µg/g). In contrast to our study, Paransa and his co-workers²⁶ (2020) found that chlorophyll-d was higher (16.36–21.42 µg/g) than chlorophyll-a (6.14–18.32 µg/g) in Kappaphycus alvarezii. This may be attributed to that chlorophyll-d can support the role of chlorophyll-a in red algae²⁷.

Phycobiliproteins (PBP) has many health advantages as antioxidants and free-radical scavengers²⁸besides their potent neuroprotective, anti-bacterial²⁸, anti-inflammatory²⁹, anti-allergic³⁰, antitumoral³¹, anti-ageing³⁰, anti-Alzheimer, immunomodulatory³², and hypocholesterolemic agents¹³. Basically, phycobiliproteins (PBP) are classified into four pigment families, according to absorption properties. Red algae comprise phycoerythrin (PE), phycocyanin (PC), allophycocyanin (APC), while phycoerythrocyanin (PEC) is absent in this group¹³. Actually, PBP have been found to be vital in proliferating and adaptimg the red algae, via maximizing the capabilities of algal light-harvesting at the deep layers in the water column¹³. In the present study, PE was not detected by the HPLC. This may be attributed to the methodologies of extraction of the PE. In the present study, the extraction process was based on adding acetone as a solvent to the dry powder alga, followed by HPLC for separation and isolation of pigments, while in many previous literature different methodologies were used to determine PE based mainly on using different buffer solutions such as phosphate buffer³⁰, sodium citrate buffer³³, and EDTA³⁴. The extraction was followed by purification, using many efficient methods like precipitation with ammonium sulfate³⁵, ion-exchange chromatography³⁶, expanded bed absorption and ion-exchange chromatography³⁷.

Considering the other two pigments, allophycocyanin content was higher (41.95 µg/g) than that of phycocyanin (20.60 µg/g) in P. gibbesii. Francavilla and his co-workers³⁸ reported that PC was the less abundant phycobiliprotein in Gracilaria gracilis, which is consistent with our results. Pina and his co-workers³⁹showed that the concentration of PC in Chondrus crispus was 149 µg/gdw, while Sukwong and his co-workers⁴⁰ isolated from Gelidium amansii 56 µg/g dw of PC. These differences in PC and APC contents compared with the previous studies may be due to many factors such as aforementioned methodologies for extraction, the species, time of the year when harvesting, or due to environmental conditions such as the light intensity⁴¹, nutrient cycles and photoperiod⁴².

Carotenoids in red algae are divided into carotenes (β-carotene and α carotenes) and the major xanthophylls (antheraxanthin, β-cryptoxanthin, lutein, violaxanthin, and zeaxanthin)⁴³. Schöbel³³ reported that rhodophytes lack distinctive carotenoid profiles due to either existence or absence of specific carotenoids, which are constituents in the xanthophyll group. On the other hand, Mimuro & Akimoto⁴⁴ noted that the existence of particular biosynthetic routes or the distribution of carotenoids with different molecular structures can be considered as an index for algae classification. In this trend, Shubert and his co-workers¹¹ estimated the carotenoid content of 65 subtropical red algal species from many taxonomic orders and families. The findings demonstrated that there were three main carotenoid profiles identified, with the exception of the Ceramiales and Corallinale. Shubert and his co-workers¹¹reported that most of the species had the lutein as the major xanthophylls (first profile), while zeaxanthin was the major one in some other species (second profile). The third profile (Xanthophyll Cycle -related carotenoids) showed that violaxanthin or antheraxanthin were also detected in some species. In addition to these major xanthophylls, there are minor ones that depend on the interconversion of the major pigments⁴⁵.

The variation in these trace pigments may be the reason of the unclear relationship between the carotenoid content of red algae and their phylogenetics⁴³. The findings of Takaichi⁴³synergized with the previous study of Czeczuga¹², where he reported in five red algal species belonging to different families different profiles of carotenoides than that of Shubert and his co-workers¹¹. Czeczuga¹²explained the different pigments profiles on the basis of the presence of additional minor xanthophylls such as γ-carotene, α-cryptoxanthin, lutein epoxide, mutatoxanthin, fucoxanthin, neoxanthin and others. Our results are in agreement with those of Czeczuga¹²and Takaichi⁴³ and disagree with those of Shubertand his co-workers¹¹. It is also noteworthy to mention that the taxonomic position of the Grateloupia, Phyllymenia and Prionitis genera remains controversial and still many species are re-identified or transferred from one family to another one. Currently, the species G. gibbesii is considered as a synonym of P.gibbesii¹⁶, which was transferred to the genus Phyllymenia based on the female reproductive structures and other attributes¹⁶. Thus, it is necessary to screen again the pigments profile of the members of order Hallymeniales, which was previously included in order Cryptomeniales and recently has undergone many taxonomic changes and may showed different pigments profiles.

In the present study, the profile of P. gibbesii showed that β-cryptoxanthin was the principle xanthophyll component (42.50 µg/g) forming 42.37% followed by the lutein (31.30 µg/g) forming 31.21% of total carotenoids, with antheraxanthin and violaxanthin forming collectively 26.42% and with the absence of zeaxanthin. On the other hand, β-carotene and α carotenes were comparable in P. gibbesii forming (80.6 µg/g) and (76.1 µg/g), contributing by 31.36% and 29.61% of total carotenoids, respectively. Thus, the percentage of total carotenes (60.97%) was higher than that of xanthophylls (39.03%). However, the content of the two carotenes are dependent on the lycopene pathway, whether it is mainly cyclized into either β-carotene or α-carotene or both⁴⁶. Also, the difference of algal species and their geographical distribution, seasonality, environmental conditions and the light regime are controlling factors of carotenoids content⁴⁷. In the present study, total carotenoids content was higher (257.00 µg/g) than chlorophyll-a (41.65 µg/g).This is consistent with the findings of Barsanti&Gualtieri⁴⁸ who reported that algal species exposed to high light intensity typically exhibit a relatively high amount of carotenoid pigments in comparison with chlorophyll-a

Total phenolics and flavonoid contents (TFC).

The acetone extract of P. gibbesii had a total content phenolics as 146.67 ± 0.61 mg/g and a total content of flavonoid was 104.40 ± 0.10 mg/g (Table 2).

Table 2

Total phenolics and total flavionoids in *P. gibbesii.*
Concentration (mg/g)	Total phenolics	Total flavonoids
Extract of P. gibbesii	146.67 ± 0.61	104.40 ± 0.10

Numerous biological actions, like antimicrobial, anti-diabetic, antioxidant, and anticancer capabilities, are provided by phenolic compounds, which include one or more phenolic rings that may be halogenated⁴⁹. The certain classes of phenolics in the red algae are bromophenols, terpenoids, phenylpropanoid derivatives polymerized hydroxycinnamyl alcohols, and mycosporine-like amino acids⁵⁰. In the current study, phenolic content in P. gibbesii was much higher (146.67 ± 0.61 mgGAE/g) than that of Shabaka & Moawad⁵¹ in the same alga during the same season (May, 2019) at the same site (Eastern Harbor) utilizing different solvents (chloroform, ethyl acetate and distilled water), resulting in (4.745, 6.629 and 3.211 mgGAE/g), respectively. The great difference between the phenolic content of the two algal samples can be attributed to the choice of the extracting solvent, where the acetone in our study showed very high efficiency than the other solvents.

The significance of total flavonoid content is mostly due to its redox properties that could explain its antioxidant, anti-inflammatory, and antibacterial properties towards many microbes⁵². In addition, the antioxidant property of the flavonoid content effectiveness is attributed to its hydroxyl groups structuring, which may be responsible for capturing and stabilizing much more free radicals⁵³. However, in the current study, flavonoid content in P. gibbesii was much higher (104.40 ± 0.10 mg CAT/g) than that of Khristi and his co-workers⁵⁴ in G. indica (0.0241QUE mg/g) using methanol as extracting solvent, while Ruiz-Medina and his co-workers¹⁰ found that flavonoid content was 1.44 mgCAE/g in G. imbricata using 80% methanol. This may be attributed to using different methodologies and different solvents and other limitations like species of algae, harvesting season, and environmental conditions⁵⁰.

Biological activities of P. gibbesii extract. The results of the biological activities of the newly recorded alga P. gibbesii are shown in Tables (3–5).

Antioxidant activity. The DPPH was a significant metric for assessing the antioxidant activity of an extract. Also, ABTS assay has been extensively used to test the ability of different extracts, fractions, and/or pure substances to scavenge free radicals.

Activity of DPPH radical scavenging. The results indicated that increasing in the extract concentration boosted the DPPH'^s capacity (Table 3). Knowingly, the better the antioxidant properties, the smaller the value IC₅₀. Indeed, it was 9.88 ± 0.01 g/mL for the P. gibbesii, while it was 3.44 ± 0.01 g/mL for the positive control (L-ascorbic acid) (Table 4).

Table 3

Antioxidant, hemolytic and anti-inflammatory activities (%) at different concentrations of *P. gibbesii* extract.
Concentration (µg/mL)	Radical scavenging activity(DPPH) (%)	Radical scavenging activity(ABTS) %	Hemolytic activity (%)	Anti-inflammatory activity (%)
10	50.62	40.31	18.75	81.25
20	56.44	45.93	29.38	70.63
40	64.36	56.54	36.00	64.00
80	70.92	79.32	44.00	56.00
100	81.44	89.62	49.88	50.13

ABTS radical scavenging assay. The results demonstrated that, like the DPPH, increasing the concentration of the acetone extract of P. gibbesii enhanced the scavenging activity scored by ABTS assay (Table 3). Moreover, the P. gibbesii acetone extract showed ABTS activity with an IC₅₀ value of 21.77 ± 0.01 µg/mL corresponding to 7.73 ± 0.01 µg/mL for L-ascorbic acid (Table 4).

Antioxidants are efficacious in safeguarding cells against ROS-mediated oxidative damage, particularly under unfavorable conditions⁵⁵. Several synthetic antioxidants are commercially available, but due to safety concerns, there has been a lot of interest in switching to natural plant-based antioxidants⁵⁶. The current data showed higher DPPH radical scavenging activity in P. gibbesii, with a maximum of 81.44%, which was higher than that of G. indica, showing a maximum of 69.90%⁵⁵. Similarly, the ABTS assay showed high activity with a maximum of 89.62%. Noticeably, the free radical scavenging capacity increased with raising up the concentration of the algal extract. This scavenging capacity may be due to the hydrogen-donating ability of the antioxidant properties of P. gibbesii⁵⁷. This might be interpreted by the view that there is a positive correlation between pigment concentration and antioxidant activity of the algae species. Increasing pigment production is induced by increasing light intensity, which in turn boosts antioxidant activity⁴¹. Furthermore, according to Zhang and his co-workers⁵⁸, the antioxidant activity of seaweeds may be influenced by the presence of flavonoids and polyphenols components. However, their concentrations affected the activity potentiality.

Table 4

Inhibitory concentrations (IC₅₀) (µg/mL), at which the algal extract showed antioxidant, hemolytic and anti-inflammatory activities.
Concentration (µg/mL)	Radical scavenging activity		Hemolytic activity	Anti-inflammatory activity
Concentration (µg/mL)	DPPH	ABTS	Hemolytic activity	Anti-inflammatory activity
Standard material	Ascorbic acid	Ascorbic acid	Aspirin	Diclofenac
(IC₅₀) of standard (µg/mL)	3.44 ± 0.01	7.73 ± 0.01	5.94 ± 0.01	331.24 ± 0.04
(IC₅₀) of P. gibbesii (µg/mL)	9.88 ± 0.01	21.77 ± 0.01	100.25 ± 0.01	99.75 ± 0.05

Hemolytic activity assay. The hemolytic activity of P. gibbesii increased gradually with the increase in the algal extract concentrations (10, 20, 40, 80, and 100 µg/mL), attaining a maximum capacity of 49.88% (Table 3). The hemolytic activity exhibited a higher IC₅₀ value of 100.25 ± 0.01 µg/mL, compared with that of Aspirin (5.94 ± 0.01 µg/mL).

Hemolysins are lipid and protein substances that cause the erythrocyte to burst and release hemoglobin, harming a number of vital organs including the heart, liver, and kidney⁵⁹. Moreover, hemolysis may result in anemia or jaundice. As a result, while testing the biological activities of algal extracts and derivatives for pharmaceutical purposes, it is necessary to investigate the hemolytic activity⁶⁰.

Herein, the hemolytic potency of the algal extract was higher (IC₅₀ = 100.25 ± 0.01 µg/mL) than that of Aspirin which represents a positive control (IC₅₀ = 5.94 ± 0.01 µg/mL). On contrast, the P. gibbesii hemolytic activity was lower than that of the red alga Hypnea cornuta extract (IC₅₀ = 1396.23 µg/mL), the green alga Ulva prolifera (IC₅₀ = 1298.25 µg/mL) and the brown alga Turbinaria triquetra (IC₅₀ = 973.68 µg/mL)⁶¹. This showed that P. gibbesii extract is better than these species for pharmaceutical purposes.

In vitro anti-inflammatory activity. The anti-inflammatory activity of P. gibbesii extract at different concentrations (10, 20, 40, 80, and 100 µg/mL) is represented in Table 3. This extract exhibited a lower IC₅₀ value of 99.75 ± 0.05 µg/mL compared with that of the commercial Diclofenac (331.24 ± 0.04 µg/mL) (Table 4). The development of many sever diseases has been linked to complicated biochemical events that distinguish the inflammation process⁶. The anti-inflammatory activity of the extracts obtained from different red algae species has been confirmed by several studies (e.g. Chen and his co-workers⁶²). Within the current study, the IC₅₀ value of the algal extract (99.75 ± 0.05 µg/mL) was much lower than that of the commercial Diclofenac (331.24 ± 0.04 µg/mL). This showed that P. gibbesii is of great potential to develop natural sources of antioxidants that may help in combating inflammatory diseases.

Antimicrobial activity. All of the examined microorganisms were susceptible to both antibacterial and anti-yeast effects of P. gibbesii acetone extract, particularly at high concentration of 0.1 mg/mL (Table 5). The extract had the greatest impact on a Gram-negative bacterium; E. coli and a yeast; C. albicans.

Table 5

Antimicrobial activity (mm) of acetone extract of *P. gibbesii*.
Microbe	Gram stain and shape	Concentration (mg/mL)/ Inhibition zone diameter (mm)			MIC
Microbe	Gram stain and shape	0.025	0.05	0.1	MIC
K.Pneumonia ATCC700603	Gram -ve, rod-shaped	11	15	18	0.025
E. coliATCC25922	Gram -ve, rod-shaped	20	26	30	0.025
S. aureus ATCC25923	Gram + ve, spherically-shaped	ND	11	18	0.05
S. pyogenesEMCC1772	Gram + ve, spherically-shaped	ND	11	15	0.05
C.albicansEMCC105	Yeast	19	21	28	0.025
- **Diameter include 5 mm well diameter.
- ND: Not detected.
- MIC: Minimum inhibition concentration (mg/ml).

Nowadays, the bioactive compounds derived from seaweed metabolites have been documented as antiviral, antibacterial, antifungal, and antiprotozoal agents⁶³.Abu-Ghannam & Rajauria⁶⁴ explained the antimicrobial mechanism in view of carotenoids role, which causes the accumulation of the immunological enzyme lysozyme that breaks down bacterial cell walls. The antimicrobial activity of P. gibbesii acetone extract was promising, where all the tested microorganisms were inhibited at different degree. This was confirmed by the minimum inhibitory concentration (MIC) (0.025 mg/L), which showed the low resistance and the high sensitivity of these microorganisms to the algal extract, particularly E. coli and C. albicans. Moreover, the efficiency of the algal extract augmented with the high concentration. In this trend, Abdel-Latif and his co-workers⁶⁵carried a study on Grateloupia doryphora, which exhibited a wide range of antimicrobial action towards the investigated microbial species namely; Bacillus subtilis, Enterococcus faecalis, Staphylococcus aureus, E. coli, Pseudomonas aeruginosa, and C. albicans. Obviously, P. aeruginosa was the most affected microbe with higher inhibition zones (30, 28 and 27 mm) for methanolic, ethanolic extracts and ethyl acetate, respectively. In addition, Negm and his co-workers⁶⁶ prepared silver nanoparticles from Grateloupia sp. showing activity versus E. coli, S. faecalis, S. aureus, P. aeruginosa, and V. damsela. Moreover, Hajri and his co-workers⁶⁷ studied the antibacterial among other biological activities for the aqueous extract of Grateloupia sparsa in the formula of cobalt oxide nanoparticles (Co₃O₄NPs). Amazingly, their data showed that Co₃O₄NPs had stronger antibacterial activity than Ciprofloxacin, a common antibiotic.

Recently, the red alga P. gibesii was newly recorded in the Mediterranean Sea of the Egyptian coast. Herein, it was investigated for phytochemical content and pigments' profile. The P. gibesii chromatograms showed ten individual photosynthetic pigments: chlorophyll-a, chlorophyll-d, α-carotene, β-carotene, phycocyanin, allophycocyanin, antheraxanthin, β-cryptoxanthin, lutein, and violaxanthin. The results of P. gibbesii acetone extract showed many biological activities including antioxidant, anti-inflammatory, and antimicrobial activity, which confirmed their potential biochemical components. As a result, the alga might be seen as a potential source of bioactive substances that can be applied in several industries, especially in pharmaceutical, biotechnological, and nutraceutical. This gives the opportunity for recycling this alien species through safe and eco-friendly manner.

Area of the study. The algal samples of newly recorded P. gibbesii were collected from the Eastern Harbor, Alexandria, Egypt during spring (May, 2019). The algal samples were collected at depth of 0.5-1 m at the Scout club, which is situated in the Eastern Harbor at 31°13.3`N latitude and 29°53.10`E longitude.

Sample collection. The algal samples were manually collected then rinsed in seawater at the site of collection to get ride the adherent sediments and other impurities before being placed in clean plastic bags. The samples were kept in an ice box at 4°C. Upon arrival at the lab, algal samples were promptly rinsed with tap water to remove any remained epiphytes and contaminants. Rodrguez-Prieto and his coworkers¹⁵ identified the newly introduced alga as Grateloupia gibbesii Harvey by using molecular and morphological analysis. It belongs to Class Florideophyceae, Order Halymeniales, Family Grateloupiaceae. The species originated from Sullivan's Island, Charleston, South Carolina¹⁵ and is currently considered to be the synonym of Phyllymenia gibbesii (Harvey) Showe M. Lin, Rodríguez-Prieto, De Clerck & Guiry 2022¹⁶.

Afterword, 250 g of the alga was air dried to a consistent weight at the ambient temperature, the algal sample was chopped into tiny chunks and grinded to a fine powder for the next procedures.

Preparation of algal extract A weight of 100 g of algal powder was macerated in 400 mL of acetone for 48 hours. In a rotating evaporator, the acetone was filtered and concentrated at 40°C under pressure. The acetone extract was then stored at -20°C for further analysis⁶⁸.

High-performance liquid chromatography (HPLC). Three groups of pigments were measured by using HPLC technique. They are namely; chlorophylls (chlorophyll-a and chlorophyll-d), phycobiliproteins (allophycocyanin, phycocyanin and phycoerythrine) and the carotenoids (α-carotene, β-carotene, antheraxanthin, lutein, β-cryptoxanthin, violaxanthin, and zeaxanthin).

High-pressure liquid chromatography was used to analyze chlorophyll-a and chlorophyll-d under isocratic conditions on the instrument (Agilent 1100 Series): C18 column with a diode array detector set at detection wavelengths (λ det.); 430 and 660 nm. The mobile phase was acetonitrile/methanol/ethyl-acetate in the ratio of 60 : 20 : 20, with flow rate; 1 mL/min, and temperature; 25°C.

Phycobiliproteins (phycoerythrin and phycocyanin) were analyzed by HPLC by using a UV detector set at detection wavelengths: 260 nm under isocratic conditions, which included the following: mobile phase- acetonitrile/methanol in the ratio of 80 : 20, respectively. The flow rate was 1 mL/min at temperature of 25^oC.

Allophycocyanin and lutein were analyzed using an HPLC system with an Echromatech Mod.C1620, column: 18 by using a detector set at 620 nm. The isocratic conditions were a Na-phosphate buffer (pH 3.0) as the solvent (A) and NaCl and methanol as the solvents (B) in the ratio of 45 : 55, respectively. The flow rate of process was 0.5 mL/min at temperature was 25^oC.

Carotenoids (α-carotene, β-carotene and zeaxanthin) were assessed by using an HPLC with a diode array detector and data collected by a Chemstation. Sample (20 mL) was loaded on ODS-1 reversed phase column (250'4.6 mm i.d., 5 mm particle size). Acetonitrile, 2-propanol, and water were eluted isocratically in the following proportions: 39 : 57 : 4. The detection wavelength was 450 nm, while the detection flow rate was 1 mL/min at temperature was 25°C.

Antheraxanthin analysis was carried out by HPLC analysis using the system echromatechMod.C1620, column: C18, with a detector set at detection wavelengths of 490 nm, and under isocratic conditions, with the mobile phase made up of methanol, water, acetonitrile, and dichloromethane in the ratio of 70 : 4 : 13 : 13. Temperature was 25°C and the flow rate was 1 mL/min. The conditions were the same for β-cryptoxanthin, except a detector set at 450 nm was used, and the mobile phase was methanol / acetone in the ratio of 70 : 30. The process detected violaxanthin used a 450 nm detector under isocratic conditions with mobile phase (A) acetonitrile / water in a ratio of 90 : 10 and mobile phase (B) was ethyl acetate. The flow rate was 1 mL/min and the temperature was 25°C.

Different standards of each pigment were utilized to prepare its calibration curve for quantification. All standards were bought from Sigma and were 95% pure (HPLC grade). The retention times and spectral data were compared to those of the authentic standards in order to identify the HPLC peaks.

Determination of total phenolic content (TPC). According to Dewanto et al.⁶⁹, Folin-Ciocalteu reagent was used to determine the total phenolic content. 200 µL of the dissolved sample (one mg of extract after being dissolved in one mL of deionized water) was added to 600 µL of distilled water, and 100 µL of Folin-Ciocalteu reagent. Before 2% Na₂CO₃ was added, the mixture was agitated and allowed to stand for 6 minutes. A final volume of 3 mL was adjusted with distilled water, which was then well mixed. The absorbance at 650 nm was measured in comparison to the produced blank after 30 minutes of incubation in the dark. A standard curve was produced utilizing various Gallic acid concentrations (standard, 0-100 µg /mL). Based on the calibration curve, the following linear equation was used to compute the total phenol content (TPC), which was expressed as Gallic acid equivalent (GAE)/mg of dry weight: y = 0.0095x − 0.0409 & R² = 0.9953. Where x is the concentration (GAE mg/g extract), y is absorbance, and R² is the correlation coefficient.

Determination of total flavonoid content (TFC). Total flavonoids of the algal extract were estimated using a modified colorimetric method published by Sakanaka et al.⁷⁰. Catechol as a standard at concentrations of 20–200 µg /mL. Precisely, 250 µL of extract or standard solutions were added to 1.25 mL of distilled water, 75 µL of 5% sodium nitrite solution (NaNO₂), and 150 µL of 10% Aluminium chloride solution (AlCl₃) five minutes later. 0.6 mL of distilled water and 0.5 mL of 1 M sodium hydroxide (NaOH) were added after 6 minutes. Afterward, the mixture was shaken well and the absorbance was determined at 510 nm. Based on the calibration curve, the following linear equation was used to assess total flavonoid content (CE): Y = 0.0079 x − 0.109 & R² = 0.986. Where R² is the correlation coefficient, X is the concentration (CE mg/g extract), and y is absorbance.

Assays determining antioxidant activity

DPPH radical scavenging activity. The 2, 2-diphenyl-1-picrylhydrazyl (DPPH) technique, developed by Brand-Williams et al.⁷¹, was modified to test the algal extract's capacity to scavenge free radicals. One milliliters of the radical solution (0.2 Mm DPPH in methanol, 0.0078 g/100 mL) was added to 1 mL of the sample, or standard solution, at various concentrations (1 : 1, v/v). The mixture was incubated at room temperature in the dark for 30 minutes, and the absorbance was detected at 517 nm. To create a calibration curve, the ascorbic acid solution was employed as the standard with a concentration range of 5-200 µg/mL. However, DPPH radical scavenging activity was qualified as mg ascorbic acid equivalent (AAE)/g dried sample. Using the following equation, the percentage of DPPH radical-scavenging activity was determined:

DPPH radical scavenging activity (% inhibition)\(=\frac{({Abs}_{Control}-{Abs}_{Sample})}{{Abs}_{Control}}\times 100\)

All reagents were added to the control sample, with the exception of the algal extract. All measurements were made in triplicate, and the average result was tabulated.

ABTS radical scavenging assay. The assay of 2,2′-Azino-bis (3-ethylbenzothiazoline-6-sulfonic acid; ABTS) was used to determine the ABTS radical scavenging activity⁷². Comparing the extract's ability to scavenge ABTS with that of dibutyl hydroxytoluene (BHT) and % inhibition Calculated as:

ABTS radical scavenging activity (%) = [(Abs.control- Abs.sample)]/ (Abs.control)] x 100

Where, Abs. sample is the absorbance of ABTS radical + sample extract/standard, whereas Abs. control is the absorbance of ABTS radical + methanol.

Hemolytic activity assay. The experiment was carried out in 2 mL microtubes via a modified Farias et al.¹⁴ method. First, a two-fold serial dilutions of each extract with 0.9% NaCl between 1,000 and 1.9 𝜇g/mL was made and set aside. Afterward, 900 𝜇L of each extract dilution were placed in a new microtube, and 100 𝜇L of a 1% red blood cell suspension (A, B, and O human blood types or rabbit blood) were added. The microtube was then incubated at 37°C for an hour. All tubes were centrifuged for 5 minutes at 3,000 ×g. A 96-well plate containing the supernatant (200 𝜇L) was connected to a microplate reader to measure different absorbances at 540 nm. The cell suspensions of each human blood type (100 𝜇L) were mixed with distilled water or 0.9% NaCl (900 𝜇L). Following is how the percentage of hemolysis was determined: % Hemolysis = Abs_test/Abs_𝑝𝑐× 100

Where Abs_pc= Abs 540 of the 1% cell suspension treated with distilled water and Abs_test= Abs 540 of the 1% cell suspension treated with sample test.

Anti-inflammatory activity assay. Using a few minor adjustments, the human red blood corpuscles (HRBCs) membrane stabilizing method⁷³ was used to evaluate extracts' anti-inflammatory activity in vitro. Blood was drawn from a healthy volunteer without using any inflammatory medications for the 14 days prior to such experiment. The blood was then transferred to heparinized centrifuge tubes and spun at a speed of 3000 rpm. After being cleaned with isosaline, the packed cells were converted into a 10% suspension in regular saline. As a reference, diclofenac potassium (50 µg/mL) was employed. About 5 mL of the reaction mixture including 1 mL of 0.15 M phosphate buffer (pH 7.4), 1 mL of test solution (1 mg/mL) in normal saline, and 0.5 mL of 10% HRBC in normal saline together with 2 mL of hypotonic saline (0.25% NaCl). One molesters of isotonic saline was adjusted as the control instead of the test solution. The mixtures were incubated for 30 minutes at 56ºC, cooled under running water, then centrifuged for 20 minutes at 3000 rpm. Using a visible spectrophotometer, the supernatant's absorbance at 560 nm was measured. The experiment was carried out three times. 100% lyses are represented by the control. The following calculation was used to compute the percentage of membrane stabilization: % Protection = 100 – (OD of test / OD of control) x 100

By graphing the percentage of inhibition with respect to the control versus the treatment concentration, the extract/drug concentration for 50% inhibition (IC₅₀) was revealed.

Antimicrobial activity assay. Reference microbial species, including; Klebsiella pneumonia ATCC 700603 and Escherichia coli ATCC 25922, were used as Gram negative bacteria. In addition, Staphylococcus aureus ATCC 25923 and Streptococcus pyogenes EMCC 1772 were used as Gram-positive bacteria. Moreover, one yeast strain (Candida albicans EMCC 105) was used. By these pathogens, the antimicrobial effect of P. gibbesii extract was evaluated.

The yeast strain was cultivated in potato dextrose broth at 28°C for 24 h, while the bacterial strains were grown in nutritional broth in g/L at 37°C. A sterile 100 mm diameter Petri plate was then filled with 100 µL of the inoculums (1×10⁸ cfu/mL) and inculcated on nutrient agar medium in g/L. The well-cut diffusion method was applied to detect the antibacterial activity⁷⁴. The wells were prepared in the plates by utilizing a cork-borer (0.5 cm) in nutrient agar plates inoculated with the reference microbes. The algal extract was added with volume of 100 µL to each well. All tested bacteria were incubated for 24 h at 37°C, while C. albicans EMCC 105 was incubated at 28°C for 3–5 days. To ascertain the minimum inhibitory concentration (MIC), P. gibbesii extract was used via setting 3 concentrations (0.025, 0.05, and 0.1 mg/mL). The diameter of the inhibition zone surrounding the well (mm) was measured in three triplicates and the average values were estimated.

Data availability

During this study, all obtained or analyzed data are included in this published article.

Acknowledgements

This paper has not funded by any financial support.

Author contributions

Regarding newly recorded algaPhyllymeniagibbesii, N.G.S.D.was in charge for this part starting from strain isolation to identification. She reviewed the previous studies in pigmentation of alga. She also collected the data, analyzed, and interpreted them, and finally, wrote the manuscript draft, and revised.Regarding algal pigments, M.M.A.H. was in charge for this part starting fromextraction to characterization using HPLC tool.Regarding the biological activities of various algal pigments, M.G.A.W., as well as, she shared the manuscript writing. Moreover, H.A.H.I. supervised all performed tasks. As well, he analyzed the obtained data, reviewed the previous studies, and finally wrote and edited the manuscript final version.

Funding

Open access funding provided by The Science, Technology & Innovation Funding Authority (STDF) in cooperation with The Egyptian Knowledge Bank (EKB).

Competing interests

The authors declare no competing interests. Additional information Correspondence and requests for materials should be addressed to H.I.

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Biological activities of derived pigments and polyphenols from newly recorded alga; Phyllymenia gibbesii

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