Elemental Composition, Antioxidant, Anti-inflammatory and Anti-genotoxic Properties of Nitophyllum punctatum

1 Introduction

Marine algae, encompassing a diverse range of photosynthetic organisms, are pivotal to oceanic ecosystems. These include microscopic phytoplankton and larger macroalgae like seaweeds (El Gamal, 2010). Macroalgae, such as kelp and red, green, and brown algae, provide habitats and nourishment for marine life. They are vital in coastal ecosystems, contributing to biodiversity and shoreline protection (Roy et al., 2022). Additionally, marine algae are economically significant and used in food, pharmaceuticals, and biofuels (Mandalka et al., 2022). Their role in biogeochemical cycles, nutrient cycling, and as bioindicators of environmental changes underscore their ecological importance (Dini, 2023). As climate change impacts marine environments, understanding and conserving marine algae is crucial for maintaining ocean health and mitigating global climate effects.

In coastal areas marine algae are found attached to rocks and other hard substrata. They are primary producers and contain chlorophyll which is a source of many nutrients, high protein content, and a rich source of dietary fibers. Some algae are used as food sources and for the preparation of beverages but the higher content of toxic elements in algal food products like cadmium or mycotoxins, limit their use as direct dietary food sources. Algae also synthesize various bioactive compounds including pigments (Wynne and Bold, 1985); by virtue of these molecules, the marine algae also possess many pharmacological properties (Neushul, 1990). The isolation of these active components has paved the way for the discovery of new anticancer drug formulations. They can also be used for the preparation of biodiesel, bioethanol, biobutanol, and some hydrogen gases (Bulgariu and Bulgariu, 2012). The algae are classified into three different groups based on color and storage of food (Garson, 1989), Brown, Green, and Red algae (Rhodophyta).

Around ten thousand species are described as red algae, belonging to the class Rhodophyceae (Wehr et al., 2015). Gelatinous filaments, free filaments, and pseudo-parenchymatous are the most common forms. The most common red algae include Irish moss, Laver, Dulse, etc. Red Algae have great ecological importance as they meet 40–60 % of total global oxygen demand (KRAFT, 1981). They also constitute the main food source in Japan and in the North Atlantic regions (El Gamal, 2010). They are a source of dietary fibers and help to promote body metabolism. One of the important groups of red algae is the Corallines algae, and coralline from it has been used in bone replacement therapies and used as vermifuges in ancient times (Naveed, 2014).

Red algae are abundant reservoirs of phenolic bioactive secondary metabolites. The spectrum of these phenolic derivatives encompasses flavonoids, simple phenolic acids, and halogenated derivatives. These bioactive elements hold significant promise in various medical applications. Flavonoids exhibit potent antioxidant properties, phenolic acids demonstrate anti-inflammatory effects, while bromophenols present diverse applications, including antimicrobial, anti-tumor, and potential antiviral activities, offering avenues for innovative therapeutic developments (Naveed, 2014). Algal polysaccharides have the potential to be exploited as an effective, non-toxic free radical scavenger that can be used to prevent oxidative damage in tissues (Kwon and Nam, 2007).

Lakshadweep has a marine ecosystem with many important marine plants and animals (Khan, 2017). Among the marine algae found, those belonging family Rhodophyceae is found in abundance. Usually, a lot of seaweeds are present in Lagoon Island like Agatti, Kavaratti, Bangaram, and Minicoy (Kaliaperumal and James, 1993). In Lakshadweep, seaweeds are special and valuable and are used as food items traditionally and also for medicines for allergy in Lakshadweep (Kaliaperumal and James, 1993). However, a very limited number of scientific studies are available on the pharmacological studies of marine algae from Lakshadweep.

In the present study, we went on to analyze the nutritional composition and biological effects of an under-explored red algae Nitophyllum punctatum. A study by Malhotra and Cojandaraj (2024) indicated the in vitro antioxidant and anti-diabetic effects of N. marginale. Similarly, the initial studies by Sridevi et al. (2003) indicated that the N. marginata contain important nutrients and therefore important source of dietary elements. There were no further studies on the pharmacological effects of the genus. Hence, we selected the plant N. punctatum for further analysis of the nutritional content and biological activities.

2 Materials and methods

2.1

2.1 Collection

The red algae of Nitophyllum punctatum (Fig. 1) belonging to the Delesseriaceae family were collected from Kavaratti island of Lakshadweep (10.5593 N, 72.6358 E). The alga was identified by Dr. Vinod K., Central Marine Fisheries Research Institute, Calicut, Kerala.

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Fig. 1

N. punctatum plant.

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3 Results

4 Discussion

Plants are important sources for bioactive secondary metabolites that are important pharmacological and nutritional agents (Uddin et al., 2019). Many of such plants are present in the diverse ecosystems of the land and known for their values in traditional and folk medicines (Mahmud et al., 2017; Muzammil et al., 2022). Several marine plants and marine sea weeds are also reported to have strong bio-pharmaceutical potentials. The algal extract widely used in Chinese medicine for treatment of various human diseases. Seaweeds are considered to be rich source of antioxidants. The anti-oxigenic activity of red algae are lower in comparison to brown algal species (Fujimoto and Kaneda, 1984). Previous studies reported that bioactive properties of read algae extract include antiviral, antifungal, anti-microbial, anti-diabetic and anti-tumour properties. Red alga Plocamium and Chondrococcus secretes polyhalogenated monoterpenes which are attributed to the antimicrobial and antitumor activity exhibited (Blunt et al., 2004). The industrial uses of the algal extract are predominantly confined on its insecticidal potentials. Dried extract of N. punctatum is used as a high potential larvicidal agent against the mosquito larvae (Elbanna and Hegazi, 2011).

The present study identified the presence of useful trace elements in N. punctatum. The trace elements, such as zinc, selenium, and copper, are crucial for maintaining health (Mehri, 2020). They function as antioxidants, protecting cells from damage, as well as have metabolic and pharmacological roles in various cellular processes (Zheng, 2020). Apart from these trace elements, the N. punctatum had higher phenolic and flavonoid contents. Phenolic compounds are importance agents that act as chain breaking antioxidants (Mittal and Raghavarao, 2018). The present study revealed that the phenolic (47.5 ± 1.55 mg GAE/ g) content was moderately low concentration. Previously, it has been reported that low concentration of phenolic compounds have been detected from the genus Gracilaria (Chen et al., 2013). Major phenolic compounds are expected to be bromo-chloro derivative and subsequently have stronger effects in the Gracillaria species (Huang and Wang, 2004). In the present study we expect the presence of phenolic compounds which are the derivatives of bromo-chloro halides, whose exact chemical nature needs to be ascertained in future studies.

In the present study the result of antioxidant assay revealed significant radical scavenging abilities against DPPH and hydrogen peroxide radicals. In the previous studies, Gracilaria showed of moderate to weak antioxidant potential (Chen et al., 2013). Similar studies on Chinese algae (Zhang et al., 2017), and Mexican algae (Zubia et al., 2009) reported antioxidant property under in vitro studies. In vivo antioxidant studies highlighted ththat chloroform extract derived from Gracilaria blodgettii Harvey has significant antioxidant potentials (Piao et al., 2014). This extract emerged as one of the most effective in mitigating oxidative and nitrosative stress induced in leucocytes. In other reports, the DPPH assay was used to test the inhibition of radical scavenging activity by the ethanolic and methanolic extract G. birdiae and G. cornea at different concentration, the result indicate that the high scavenging activity of ethanolic extract of G. birdiae (Huang and Wang, 2004).

Further, the anti-inflammatory activities of the algal extract were evident from nitric oxide radical scavenging and Raw 264.7 cells. Previous studies by Coura et al. (2015)) indicated a sulfated polysaccharide fraction extracted from Gracilaria cornea exhibits anti-inflammatory activity by inhibiting the release of histamine, blocking migration of neutrophils, and reducing vascular permeability. The compound R-phycoerythrin derived from various red seaweeds demonstrated substantial anti-inflammatory properties (Lee et al., 2017). Hence, the anti-inflammatory properties of the plant may be helpful to yield novel antioxidant and anti-inflammatory compounds in future.

Further, our study found no notable genotoxicity at various concentrations of the algal extracts. Conversely, exposure to EMS, a genotoxic agent, triggered significant genotoxic effects in allium cells, including sticky chromosomes, mitotic spindle irregularities, and breakage in Allium cepa. On contrary, the pre-treatment with the algal extracts protected against the EMS-induced genotoxicity in A. cepa root cells. Furthermore, our investigation revealed elevated levels of polyphenols and flavonoids in the algal extract, suggesting their potential role in conferring protection against free radicals and showcasing anti-inflammatory properties. This not only adds to our understanding of novel bioactive compounds but also hints at their potential for antioxidant, genotoxicity, and anti-inflammatory effects.

5 Conclusions

In conclusion, the methanol extract obtained from the red algae N. punctatum exhibits promising antioxidant, anti-inflammatory and anti-genotoxic effects. The elemental composition analysis reveals the presence of essential minerals, highlighting its potential nutritional value. The extract demonstrates significant inhibition of nitric oxide production and downregulation of pro-inflammatory cytokines, indicating its anti-inflammatory potential. Moreover, using the Allium cepa model, the extract shows a dose-dependent reduction in DNA damage, indicating its anti-genotoxic activity. Overall, the research on the elemental composition, anti-inflammatory, and anti-genotoxic properties of the methanol extract from N. punctatum sheds light on its pharmacological importance and paves the way for further investigations and applications in the fields of pharmaceuticals, nutraceuticals, and functional foods.

Funding

The authors acknowledge the funding support from Researchers Supporting Project Number (RSP2024R11), King Saud University, Riyadh, Saudi Arabia.

CRediT authorship contribution statement

N.P. Ifrath Jahan: Writing – original draft, Visualization, Resources, Methodology, Investigation, Formal analysis. Joice Tom Job: Writing – review & editing, Writing – original draft, Supervision, Software, Resources, Investigation, Funding acquisition, Conceptualization. Ahmed Alfarhan: Writing – review & editing, Visualization, Supervision, Software, Resources, Project administration, Methodology, Investigation, Funding acquisition, Data curation, Conceptualization. Rajakrishnan Rajagopal: Writing – original draft, Visualization, Validation, Resources, Methodology, Investigation, Data curation, Conceptualization. Vinod Kavungal: Writing – review & editing, Supervision, Software, Resources, Project administration, Investigation, Formal analysis, Conceptualization. Eliza Oprea: Writing – review & editing, Visualization, Supervision, Project administration, Methodology, Funding acquisition, Data curation, Conceptualization. Arunaksharan Narayanankutty: Writing – review & editing, Writing – original draft, Visualization, Validation, Supervision, Software, Resources, Project administration, Methodology, Investigation, Funding acquisition, Data curation, Conceptualization.