Bioactive potential and chemical profile of extracts of Psidium oligospermum Mart. ex DC. (Myrtaceae)

Potencial bioativo e perfil químico de extratos de Psidium oligospermum Mart. ex DC. (Myrtaceae)

Abstract

Bioactive compounds from species of the genus Psidium have shown significant pharmacological properties, becoming promising alternatives for the development of therapeutic strategies for numerous pathologies. Psidium oligospermum Mart. Ex DC (Myrtaceae) is among species of this genus whose extracts have not been investigated in phytochemical or biological studies, making it a potential source of bioactive compounds. This objective of this study was to investigate properties bioactive of stem and leaf extracts of P. oligospermum using different solvents (hexane, ethyl acetate, and ethanol). Antimicrobial potential, antioxidant activity, and effects on cell viability were evaluated, as well as concentrations of total phenolics and flavonoids and other chemical parameters. The extracts inhibited Gram-positive bacteria (Staphylococcus aureus and Micrococcus luteus), Gram-negative bacteria (Pseudomonas aeruginosa and Salmonella choleraesuis), and fungi (Candida albicans and Candida glabrata) by the disk diffusion and minimum inhibitory concentration methods, with bactericidal activity for Gram-positive bacteria. The extracts showed antioxidant effects, with reductions of up to 84% in DPPH free radicals. The absence of toxicity in extracts obtained with ethanol and ethyl acetate was observed through hemolytic tests with sheep erythrocytes and viability tests using Artemia salina, whereas the hexane leaf extract showed moderate toxicity. The bioactivity of the extracts is related to the presence of different classes of phytochemicals such as alkaloids, triterpenoids, steroids, saponins, anthraquinones, phenols, and flavonoids. These findings provide important chemical and pharmacological information indicating that Psidium oligospermum is a promising source of compounds with therapeutic properties; however, further research using other evaluation techniques is needed.

Keywords:
antimicrobial activity; toxicity and DPPH free radicals

Resumo

Compostos bioativos de espécies do gênero Psidium têm demonstrado propriedades farmacológicas significativas, tornando-se alternativas promissoras para o desenvolvimento de estratégias terapêuticas para inúmeras patologias. Psidium oligospermum Mart. Ex DC (Myrtaceae) está entre as espécies deste gênero cujos extratos não foram investigados em estudos fitoquímicos ou biológicos, tornando-se uma fonte potencial de compostos bioativos. O objetivo deste estudo foi investigar as propriedades bioativas de extratos de caule e folhas de P. oligospermum usando diferentes solventes (hexano, acetato de etila e etanol). O potencial antimicrobiano, a atividade antioxidante e os efeitos na viabilidade celular foram avaliados, bem como as concentrações de fenólicos e flavonoides totais e outros parâmetros químicos. Os extratos inibiram bactérias Gram-positivas (Staphylococcus aureus e Micrococcus luteus), bactérias Gram-negativas (Pseudomonas aeruginosa e Salmonella choleraesuis) e fungos (Candida albicans e Candida glabrata) pelos métodos de difusão em disco e concentração inibitória mínima, com atividade bactericida para bactérias Gram-positivas. Os extratos apresentaram efeitos antioxidantes, com reduções de até 84% nos radicais livres DPPH. A ausência de toxicidade nos extratos obtidos com etanol e acetato de etila foi observada por meio de testes hemolíticos com eritrócitos de carneiros e testes de viabilidade usando Artemia salina, enquanto o extrato de folhas hexânicas apresentou toxicidade moderada. A bioatividade dos extratos está relacionada à presença de diferentes classes de fitoquímicos, como alcaloides, triterpenoides, esteroides, saponinas, antraquinonas, fenóis e flavonoides. Essas descobertas fornecem informações químicas e farmacológicas importantes, indicando que P. oligospermum é uma fonte promissora de compostos com propriedades terapêuticas; no entanto, pesquisas adicionais usando outras técnicas de avaliação são necessárias.

Palavras-chave:
atividade antimicrobiana; toxicidade e radicais livres DPPH

1. Introduction

Plants produce various organic molecules through secondary metabolism, which generally has high structural diversity and exhibit multiple bioactivity (Wink, 2015). Many compounds have been identified, extracted, and isolated from species of the genus Psidium and widely evaluated for their biological activity, generating a large number of research publications worldwide (Díaz-de-Cerio et al., 2017; Lok et al., 2023; Chechani et al., 2024; Gwozdz et al., 2022).

Psidium is the fourth genus in number of species in the Neotropical region (Proença et al., 2022), including important botanical species, such as Psidium guajava. Many metabolites have been isolated from different representatives of this genus. There are approximately 72 phenolic compounds recorded for P. guajava (Díaz-de-Cerio et al., 2016; Ugbogu et al.,, 2022; Rojas-Garbanzo et al., 2017), 17 triterpenoids, 30 flavonoids, 19 sesquiterpenoids (Jiang et al., 2020), and 14 meroterpenoids (Qin et al., 2017), and other phytocompounds, including carotenoids, tannins, saponins, and alkaloids (Morais-Braga et al., 2016; Bhagavathy et al., 2018; Alhaidari et al., 2019). Additionally, 50 compounds were found in essential oil of P. guajava (Wang et al., 2017).

Phenolic compounds, such as myricetin, quercetin, quercitrin, and ellagic acid, were also reported for P. friedrichsthalianum (Flores et al., 2013). Moreover, Mallmann et al. (2020) identified dozens of phenolic compounds in two P. Cattleianum varieties. These phenolic compounds include acid gallic, epicatechin, quercetin, myricetin, catechin (Medina et al., 2011; Pereira et al., 2020), anthocyanins, as cyanidin-3-o-glucoside and malvidin-3-o-glucoside (Nora et al., 2014). Phenolic compounds were also identified in pulp and seeds of P. myrtoides, including quercetin and pyrogallol as the most abundant compounds (Cassiano et al., 2024).

In this sense, studies have indicated that phenolic compounds are one of the most abundant phytochemical groups and have beneficial effects to human health, reducing the risk of development of several cardiovascular, carcinogenic, and neurodegenerative diseases, mainly due to their antioxidant effects (Pereira et al., 2018; Qin et al., 2023). Furthermore, these compounds may show antimicrobial activity by inhibiting cell wall formation, hindering biofilm formation (Bhagavathy et al., 2018), altering cell membrane permeability (Herrmann and Wink, 2011), inhibiting protein and nucleic acid synthesis (Wink, 2015), suppressing toxins (Morais-Braga et al., 2017), and having cytotoxic effects on several lines of microorganisms, including Shigella flexneri (Hirudkar et al., 2020), Salmonella enteritidis (Arima and Danno, 2002), Staphylococcus aureus (Chakraborty et al., 2018; Lima et al 2020), Pseudomonas aeruginosa (Alhaidari et al., 2019), and Escherichia coli (Abdelrahim et al., 2002; Metwally et al., 2010). These infectious agents have been among the main medical concerns, particularly in hospital settings, due to their resistance to conventional antibiotics, encouraging the search for new antimicrobial agents, mainly from natural sources (Pereira et al., 2023).

Other biological properties of medical relevance were also identified for the genus Psidium, including anti-inflammatory (Choi et al., 2008; Han et al., 2011; McCook-Russell et al., 2012; Zhang et al., 2021), immunomodulator (Kaileh et al., 2007), antidiabetic (Mukhtar et al., 2006), antiperistatical (Machado et al., 2018), antiviral (Mao et al., 2010), anticancerogenic (Lok et al., 2023), and analgesic (Alvarenga et al., 2013) activities.

Considering the vast bioactive potential of the genus Psidium, this work aimed to investigate the phytochemical properties of P. oligospermum, a species not previously studied. The study sought to answer the hypothesis that leaf and stem extracts of P. oligospermum have antimicrobial, antioxidant, and low cytotoxic.

2. Material and Methods

2.1. Collection and identification of plants

Samples of the species Psidium oligospermum were collected from a remnant Atlantic Forest area on the campus II of the State University of Bahia (UNEB), in Alagoinhas, BA, Brazil (12°10'42.62''S, 38°24'39.52'W). The plant was identified by taxonomic comparison with a specimen maintained in the UNEB herbarium collection (HUNEB), where it was deposited and cataloged under number 14668.

2.2. Plant extract

Stem and leaves of P. oligospermum plants were separated, dried at 40 °C and then crushed. Extracts were obtained by percolation using three different solvents: hexane (Neon, 01512), ethyl acetate (Neon, ref. 00057), and ethanol (Neon, ref. 03467). Each extraction was prepared with three consecutive percolation replications, with 72-hour intervals. After complete removal of the solvents, the extracts were stored at -4 °C.

2.3. Antimicrobial activity evaluation

2.3.1. Disk diffusion

Antimicrobial properties were assessed using the disk diffusion method, following the recommendations of the Clinical and Laboratory Standards Institute (CLSI, 2015). The extracts were tested against bacterial and fungal strains from the American Type Culture Collection (ATCC^®): Staphylococcus aureus (6538), Bacillus subtilis (6633), Micrococcus luteus (10240) Pseudomonas aeruginosa (15442), Escherichia coli (94863), Salmonella choleraesuis (14028), Aspergillus niger (16404), Candida albicans (18804), and C. glabrata (728). Bacteria were cultured on Müeller-Hinton Agar (HIMEDIA, ref. M173-500G) at 37 °C for 24 hours, whereas fungi were cultured on Sabouraud Dextrose Agar (KASVI, ref. K25-610103) at 37 °C for 48 hours. Subsequently, 5 mm diameter filter paper disks, impregnated with 10µL of plant extracts (100 mg mL^-1 in DMSO) were applied to the agar inoculated with the test microorganisms. Disks impregnated with 30µg of chloramphenicol (LbLaborclin^®) and disks with ciclopirox olamine (0.1%) were used as positive controls in bacterial and fungal assays, respectively; 5% dimethyl sulfoxide (DMSO) was used as the negative control. The antimicrobial activity was determined by measuring the zones of inhibition immediately after the incubation period.

2.3.2. Minimum inhibitory concentration (MIC)

MIC was determined according to the protocol described in the Clinical and Laboratory Standards Institute (CLSI, 2015). For bacterial culture, the 13g of Nutrient Broth (HIMEDIA, ref. M002-500G) for 1000 mL of distilled water, while fungi were cultured in culture broth prepared with 3g yeast extract (KASVI, ref. K25-1736), 10g triptona (KASVI, ref. K25-1041), and 3g malt extract (KASVI, ref. K25-1708) for 1000mL. Thus, 100µl of the culture medium was distributed into microplates followed by the addition of 100µl of extract and serial dilution (1:2 dilution). Microbial inoculum was added, resulting in a volume of 200µl per well (2.0 to 3.9µg mL^-1). Chloramphenicol and 5% DMSO were used as positive and negative controls, respectively. Cell viability was assessed after incubation at 37 °C for 24 hours (bacteria) or 48 hours (fungi) by applying 20µl (0.5 mg mL^-1) of MTT (3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide) in each well and incubating at 37 °C for 3 hours. Extracts with MIC between 50 and 500µg mL^-1 were considered highly active; between 600 and 1500µg mL^-1 were considered moderately active; and those greater than 1500µg mL^-1 were considered weakly active (Sartoratto et al., 2004).

Inhibitory activity was classified as microbicidal or microbiostatic by transferring 10μL of inoculum from wells showing no microbial growth to sterile media (Müeller-Hinton agar and Sabouraud Dextrose Agar), as described by Santurio et al. (2007). All microbiological tests were performed in triplicate, with three replications.

2.3.3. Phytochemical characterization and proton nuclear magnetic resonance (¹H-NMR) spectroscopy

Phytochemical analysis of extracts was performed in triplicate, as described by Matos (2009). The presence of chemical compounds in the extracts was determined using specific reagents for the detection of alkaloids (Dragendorff), steroids, triterpenoids (Liebermann-Buchard), anthraquinones, and coumarins (5% KOH solution) followed by readings under ultraviolet light at 365 nm. The presence of saponins in the extract was determined by shaking the extract in a vortex and observing foam formation. Total phenol contents in the extracts were determined by spectrophotometry using the Folin-Ciocalteu reagent at 620 nm, and expressed as milligrams of gallic acid equivalents per gram of crude extract (mg GAE g^-1). Flavonoid contents were determined as described by Arvouet-Grand et al. (1994), with adaptations for spectrophotometry at 492 nm, and expressed as micrograms of quercetin equivalents per 100 milligram of extract (µg QE 100 mg^-1). Tests for obtaining proton nuclear magnetic resonance (¹H-NMR) spectra was performed using a 500 MHz INOVA spectrometer, with tetramethylsilane (TMS) as an internal standard.

2.3.4. Antioxidant activity

The antioxidant activity of the extracts was evaluated by the reduction of activity of 2,2-diphenyl-1-picrylhydrazyl (DPPH) free radical scavenging method, based on the decrease in absorbance of each sample, as described by Brand-Willians et al. (1995). Absorbance readings were taken on a spectrophotometer (Sirus S Radim) at 492 nm, using ascorbic acid as standard. The obtained absorbances were used to determine the antioxidant capacity of the extracts, expressed as the percentage of DPPH free radical scavenging activity (%RSA), using the formula %RSA = [(Abs_sample - Abs_control) × 100] / Abs_control, where Abs_control is the absorbance of the control (DPPH radicals and ethanol), and Abs_sample is the absorbance of the extract after reaction with DPPH radicals (Ashraf et al., 2016).

2.3.5. Toxicity tests

Toxicity of the extract was evaluated based on their hemolytic activity, as described by Kalegari et al. (2011) and upon the survival level of nauplii of Artemia salina Leach, as described by Meyer et al. (1982). All tests were performed in triplicate.

Hemolytic activity was evaluated using two methodologies. The was disk diffusion on blood agar plates, where extracts were tested at concentrations of 1000, 100, and 10µg mL^-1; DMSO and Tween 80 were used ​​as negative and positive controls, respectively; and the formation of hemolytic zones was evaluated after 24, 48, and 72 hours. The second methodology consisted of using 2% hemolytic suspension with defibrinated sheep blood (Laborclin^®) and the extracts at concentrations of 1000, 500, 200, 100, and 10µg mL^-1. The suspension was slightly shaken, left to rest for 30 minutes, homogenized, left to rest for 150 minutes at room temperature, and then centrifuged at 3,000 rpm for 5 minutes. Distilled water was used as a positive control, and DMSO and saline solution were used as negative controls. Hemolysis was evidenced by the reddish hue of the plasma fraction.

The effects on A. salina were assessed by adding the extracts at concentrations of 1000, 100, and 10µg mL^-1 to 6-well plates with 10 A. salina nauplii in each well. DMSO and seawater were used as negative controls. Nauplii showing no mobility were counted within 24 and 48 hours of exposure to extract concentrations. Toxicity of the extracts was categorized based on their lethal concentration for 50% of the individuals, according to Clarkson et al. (2004), as follows: non-toxic (LC₅₀ > 1,000µg mL^-1), low toxicity (LC₅₀ > 500µg mL^-1), moderate toxicity (500 < LC₅₀ < 100µg mL^-1), or high toxicity (LC₅₀ < 100µg mL^-1).

2.3.6. Statistical analysis

Statistical analyses were conducted using Past 4.0 software. The normality of data distribution was assessed using the Shapiro-Wilk test at a 5% significance level. Normally distributed data were analyzed using one-way ANOVA, followed by pairwise comparisons using the Tukey's test at a 5% significance level. Non-normally distributed data were analyzed ​​by pairwise comparisons using the non-parametric Mann-Whitney U test at a significance level of p < 0.05. Individual analyses of isolated groups were carried out to determine the 95% confidence interval using the t-test.

3. Results

3.1. Antimicrobial activity of Psidium oligospermum extracts

P. oligospermum extracts showed activity against Gram-positive bacteria (Staphylococcus aureus and Micrococcus luteus) and Gram-negative bacteria (Pseudomonas aeruginosa and Salmonella choleraesuis) using the disk diffusion method. Stem extracts obtained with ethyl acetate and ethanol solvents were the most active, forming inhibition zones of up to 18.7 mm for M. luteus, 16.3 mm for S. aureus, and 12.0 mm for P. aeruginosa and S. choleraesuis (p < 0.05) (Figure 1).

Figure 1
Inhibition halos presented by extracts obtained in ethyl acetate and ethanol from Psidium oligosperumum against: (A) Staphylococcus aureus; (B) Micrococcus luteus; (C) Pseudomonas aeruginosa and (D) Candida albicans.

The yeast C. albicans exhibited sensitivity to all P. oligospermum extracts, with inhibition zones ranging from 9.2 to 15.7 mm, whereas C. glabrata exhibited low sensitivity to leaf extracts obtained with hexane and ethyl acetate, forming inhibition zones of 7 mm (Table 1).

Table 1
Mean size of zones of microbial growth inhibition (100 mg mL^-1) for Psidium oligospermum extracts (stems – ST; and leaves – LE).

	EXT	M. luteus	S. aureus	P. aeruginosa	S. choleraesuis	C. albicans	C. glabrata
ST	HEX	14.2 ± 2.9 b	11.1 ± 2.6 b	9.8 ± 3.9 a/b/c	9.2 ± 1.9 b/c	9.2 ± 0.7 c	-
	ACE	18.2 ± 1.8 a	12.3 ± 1.5 b	12.0 ± 1.9 a	12.0 ± 1.0 a	15.7 ± 1.1 a	-
	ETH	18.7 ± 1.3 a	16.3 ± 2.6 a	11.0 ± 1.1 a	11.6 ± 1.4 a/b	14.1 ± 2.5 b	-
LE	HEX	7.2 ± 0.9 c	7.4 ± 0.7 c	-	7.0 ± 0.8 d	9.4 ± 2.1c	7.0 ± 0 a
	ACE	14.3 ± 1.4 b	10.7 ± 1.3 b	8.3 ± 0.9 b/c	8.3 ± 0.8 c	13.0 ± 2.3 b	7.0 ± 0 a
	ETH	16.2± 2.4 a/b	12.4 ± 2.2 b	9.4 ± 1.0 b	10.0 ± 0.6 b	13.7 ± 1.3 b	-
CO	CHL	28.3 ± 2.3	28.3 ± 1.2	22.2 ± 2.3	20.7 ± 0.9
	CIC					15.3 ± 1.2	16.0 ± 0.8

• EXT = extracts; CO = Controls; CHL = chloramphenicol; CIC = ciclopirox; (-) = absence of growth inhibition; HEX: Hexane; ACE = ethyl acetate; ETH = ethanol. M. luteus = Micrococcus luteus; S. aureus = Staphylococcus aureus; P. aeruginosa = Pseudomonas aeruginosa; S. choleraesuis = Salmonella choleraesuis; and C. albicans = Candida albicans. Means followed by the same letter in the columns are not significantly different from each other by the non-parametric Mann-Whitney U test (p < 0.05).

Microdilution tests showed that P. aeruginosa was susceptible to all extracts, which showed the best results, with minimum inhibitory concentrations (MIC) between 62.5 and 250µg mL^-1 (Table 2). Regarding the viability test for this bacterium, all extracts showed bacteriostatic activity. Extracts at high concentrations had bactericidal effects on Gram-positive bacteria, except for hexane stem extract against M. luteus. Ethyl acetate leaf extracts showed MIC of 125µg mL^-1, with fungicide effect on C. albicans.

Table 2
Minimum inhibitory concentration (µg mL^-1) and type of activity of Psidium oligospermum extracts (stems and leaves) against bacteria and fungi.

	Extracts	M. luteus	S. aureus			P. aeruginosa		C. albicans
	HEX	500	BT	500	BC	250	BT	-
Stems	ACE	2000	BC	750	BC	125	BT	-
	ETH	1000	BC	750	BC	125	BT	-
	HEX	250	BC	250	BC	125	BT	-
Leaves	ACE	125	BC	750	BC	62.5	BT	125	FC
	ETH	-		1.000	BC	125	BT	-
Controls	CHL	62.5		62.5		31.25		-

• (-) = absence of growth inhibition; HEX: Hexane; ACE = ethyl acetate; ETH = ethanol; CHL = chloramphenicol; BC = bactericidal; BT = bacteriostatic; FC = fungicide; M. luteus = Micrococcus luteus; S. aureus = Staphylococcus aureus; P. aeruginosa = Pseudomonas aeruginosa; and C. albicans = Candida albicans.

3.2. Phytochemical characterization

Phytochemical tests showed the presence of alkaloids, triterpenoids, steroids, saponins, and anthraquinones, but the absence of coumarins (Table 3). Higher contents of phenolic compounds were found for hexane and ethyl acetate leaf extracts (92.19 and 88.83 mg GAE g^-1, respectively). The extracts showed high flavonoid contents, with extraction of up to 90.02µg QE 100 mg^-1 when using ethyl acetate as solvent (p < 0.05).

Table 3
Phytochemical screening of Psidium oligospermum extracts.

	EXT	AL	TRI	STE	SAP	COU	ANT	Phenols (mg GAE g-1)		Flavonoids (µg QE 00 mg-1)
Stems	HEX	+	+	-	-	-	-	68.88 ± 0.009	B	56.97 ± 0.04	C
	ACE	+	+	-	-	-	+	41.11 ± 0.0005	BC	89.93 ± 0.03	A
	ETH	+	+	-	+	-	+	31.79 ± 0.001	C	73.29 ± 0.02	B
Leaves	HEX	+	-	-	-	-	-	92.19 ± 0.009	A	71.80 ± 0.17	ABC
	ACE	-	-	+	-	-	-	88.83 ± 0.006	A	90.02 ± 0.06	A
	ETH	+	+	-	+	-	+	27.81 ± 0.001	D	44.50 ± 0.03	C

• EXT = extracts; HEX: Hexane; ACE = ethyl acetate; ETH = ethanol; AL= alkaloids; TRI = triterpenoids; STE = steroids; SAP = saponins; COU: coumarins; ANT = Anthraquinones; (+) = present; (-) = absent. Means followed by the same letter in the columns are not significantly different from each other by the Tukey's test (p < 0.05).

3.3. Proton nuclear magnetic resonance (¹H-NMR) spectroscopy

The analysis of ¹H-NMR spectra of leaf and stem extracts in ethyl acetate showed signals characteristic of several common metabolites; signals indicating the presence of terpenoid or steroid compounds with olefinic hydrogen at δ 5.32 to 5.38 ppm; methine and methylene signals between δ 1.2 and 3.5 ppm; and methyl signals from the steroid nucleus between δ 1.039 and 0.70 ppm (singlets). Additionally, the spectra showed signals indicating the presence of protons characteristic of aromatic compounds, between 6.0 and 8.0 Hz, and signals of aromatic rings containing chelating hydroxyls between 8.0 and 13.0 Hz (Figure 2).

Figure 2
Proton nuclear magnetic resonance (¹H-NMR) spectra at 500 MHz, using deuterated chloroform (CDCl₃), of extracts from stems (A) and leaves (B) of Psidium oligospermum obtained with ethyl acetate solvent.

3.4. Antioxidant activity

P. oligospermum extracts neutralized DPPH free radicals. Hexane, ethyl acetate, and ethanolic extracts presented percentage of DPPH free radical scavenging activity of 63.63±5.75, 79.89±3.61, and 84.94±1.72, respectively, for stem extracts, and 41.04±2.21, 75.83±2.28, 84.18±1.61, respectively, for leaf extracts. The highest percentages were found for ethanolic extracts.

3.5. Toxicity of extracts

P. oligospermum extracts did not show toxicity to erythrocytes. The extracts were non-toxic to A. salina nauplii, except for hexane leaf extract, which was moderately toxic, with an LC₅₀ of 158.49µg mL^-1.

4. Discussion

Similar to other species in the genus Psidium, extracts of P. oligospermum demonstrate high bioactive potential, indicating the presence of active compounds. While antimicrobial and antioxidant activities are already documented in other Psidium species, this study marks the comprehensive bioactive characterization of P. oligospermum extracts.

Extracts of P. oligospermum contain compounds exhibiting antimicrobial activity against both Gram-positive and Gram-negative bacteria, as well as fungi, demonstrating a broad spectrum of inhibition. These findings align with previous reports on other species within the genus Psidium (Lima et al., 2020; Pereira et al., 2023; Lahlou et al., 2022; Biswas et al., 2013; Qabaha, 2013; Desoti et al., 2011; Nair and Chanda, 2007; Morais-Braga et al., 2016).

During the disk diffusion assay, antimicrobial activity against Staphylococcus aureus was observed, with inhibition zones of up to 16.3 mm. These data show a similar pattern to findings in other Psidium species, such as P. guajava extracts (Raj et al., 2020; Pereira et al., 2023; Saleh and Al-Mariri, 2020; Lahlou et al., 2022; Nair and Chanda, 2007) and P. cattleianum (Lima et al., 2020).

Staphylococcus aureus is recognized as an opportunistic pathogen that can cause a range of potentially fatal infections, including those acquired in hospital and community settings. The escalating resistance of this bacterium to common antibiotics, particularly methicillin, poses a serious public health challenge (Chakraborty et al., 2018). Therefore, the chemical compounds in the evaluated extracts may provide a promising alternative for addressing these issues.

Micrococcus luteus is another important pathogen, though reports of human infections are rare, immunosuppressed patients are susceptible and may develop conditions such as endocarditis (Shi et al., 2023; Khan et al., 2019). The extract of P. oligospermum has also been reported to exhibit antimicrobial effects against M. luteus. These data are consistent with previous studies of the genus, which demonstrated inhibition of M. luteus with zones of 16 mm and 18.7 mm for extracts of P. cattleianum (Souza et al., 2004) and P. guajava (Qabaha, 2013) extracts respectively.

The effect of P. oligospermum extracts on Gram-negative microorganisms was similar to that reported for P. guajava extracts, which inhibited the growth of P. aeruginosa, with inhibition zones from 12 mm (Hoque et al., 2007) to 16.3 mm (Bona et al., 2014; Raj et al., 2020). Pseudomonas aeruginosa is an opportunist pathogen that often causes both acute and chronicle infections based on biofilm formation and is one of the main causes of difficult-to-treat nosocomial infections (Mulcahy et al., 2014; James et al., 2008; Fazli et al., 2009; Burmølle et al., 2010). Moreover, it has various virulence factors and determinants for antibiotic resistance, which contribute to its pathogenesis and are responsible for its metabolic and adaptive flexibility to different conditions, including the host's immune response (Jurado-Martín et al., 2021; Francis et al., 2017; Botelho et al., 2019).

Psidium oligospermum extracts efficiently inhibited the growth of S. choleraesuis. This observation aligns with previous reports on the antimicrobial effects of Psidium species against microorganisms of the genus Salmonella. For instance, the inhibition of Salmonella enteritidis by P. guajava (Arima and Danno, 2002) and P. cattleianum (Medina et al., 2011) extracts have been previously demonstrated. Similarly, another species, Salmonella typhi, was reported to be inhibited by P. brownianum extracts (Cordeiro et al., 2020). However, no antimicrobial activity against Escherichia coli was observed in the tests, which is consistent with the findings of Araújo et al. (2014) and Kidaha et al. (2013).

According to Sartoratto et al. (2004), the antimicrobial activity through the broth microdilution assay is considered high when the MIC is between 50 and 500 µg mL-1; moderate when the MIC is between 600 and 1500 µg mL-1; and low when the MIC is greater than 1500 µg mL-1. Therefore, the results of this study indicate that the ethyl acetate leaf extract of P. oligospermum presents high antibacterial activity against P. aeruginosa (with a MIC of 62.5 µg mL-1) acting with a bacteriostatic effect. These findings differ from the results observed for P. guajava, which indicated considerably higher MIC values ​​for P. aeruginosa (Sanches et al., 2005; Cheruiyot et al., 2009; Khan et al., 2023). The antimicrobial test also demonstrated inhibition S. aureus growth, with similar proportions to the reported by Sanches et al. (2005) and lower than the findings of Pereira et al. (2023), both testing leaves extracts of P. guajava.

Noteworthy antifungal activity was also observed against Candida albicans, in agreement with previous studies. For instance, assays with extract methanolic leaf the P. guajava demonstrated an MIC of 50µg mL-1 (Dhiman et al., 2011). However, antimicrobial activity against C. albicans can vary greatly among studies, depending on the chemical composition, extraction methods, and solvents used. In some cases, higher MIC values were reported for P. guajava extracts (Ferreira et al., 2013). Disk diffusion tests also showed comparable zones of inhibition for P. oligospermum, zones of 10–18 mm for example were observed for P. guajava (Fonseca and Botelho 2010; Nair and Chanda, 2007; Padrón-Márquez et al., 2012; Raj et al., 2020), although larger zones of inhibition have already been reported by Qabaha (2013).

In addition to the antimicrobial activity, the phytochemical composition of P. oligospermum further highlights its bioactive potential by the presence of several secondary metabolites found in the extracts. The phytochemical tests showed the presence of alkaloids, triterpenoids, steroids, saponins, anthraquinones, phenolic compounds, and flavonoids, all with records of important biological and pharmacological activities. These results are consistent with those found for other representatives of the genus, including P. bahianum (Rocha et al., 2021), P. myrsinites DC. (Durães et al., 2017), P. cattleianum (Alvarenda et al., 2015; Desoti et al., 2011; Müller et al., 2012), and P. guajava (Biswas et al., 2013; Kumar et al., 2013; Morais-Braga et al., 2016; Chechani et al., 2024).

Concentrations of total flavonoids and phenols were also consistent with records found in the literature. The extraction rate of total phenol contents was higher for the hexane leaf extract (92.19 mg GAE g^-1). Rocha et al. (2021) found similar results for leaf extracts of P. bahianum (110.57 mg GAE g^-1), whereas Pereira et al. (2023) found higher results for P. guajava (17.02±6.87 mg g^-1 of dry extract). However, other studies found significantly higher contents of these compounds in leaf extracts of P. guajava, with 575.3 mg g^-1 (Qian and Nihorimbere, 2004) and 256.32±4.56 mg GAE g^-1 (Raj et al., 2020).

Ethyl acetate extracts showed the highest flavonoid contents (up to 90.02µg QE 100 mg^-1). This is a similar result to that reported by Rocha et al. (2021) (105.36µg QE 100 mg^-1) and higher than that found for fruits of P. cattleianum and P. guajava (712 and 308µg QE g⁻¹, respectively) (Luximon-Ramma et al., 2003; Pereira et al., 2018). However, these quantitative differences may be due to the methodology and chemical solvents used in the extraction process, as well as epigenetic conditions such as environment and climate (Vargas-Alvarez et al., 2006; Luximon-Ramma et al., 2003; Pereira et al., 2018; Ashraf et al., 2016; Biegelmeyer et al., 2011).

Moreover, P. oligospermum extracts have important antioxidant properties, denoting a potential therapeutic application. Plant extracts obtained with ethyl acetate and ethanol acted as mitigators of DPPH free radicals, presenting antioxidant activity of up to 84.94%. This confirms previous studies that reported high antioxidant potential for Psidium species (Cassiano et al., 2024; Pereira et al., 2021; Lahlou et al., 2022; Aminu et al., 2012; Zahin et al., 2016). This property may be related to the amount of bioactive compounds in the extracts, such as phenolic compounds, mainly flavonoids, the main phytochemical compounds responsible for this activity (Cassiano et al., 2024; Lahlou et al., 2022; 2019), which can be attributed to the action of compounds as the quercetin, quercetin-3-O-glucopyranoside and morin (Tachakittirungrod et al., 2007), polysaccharides (Luo et al., 2019), and phenolic acids such as the ferulic acid (Chen and Yen, 2007), isolated compounds that contribute significantly to the antioxidant activity in P. guajava. However, the diversity and complexity of compounds in the extracts indicate that this activity may also be attributed to another group of chemical compounds or the combination of the main compounds in the plant extract.

Understanding the potentially toxic effects of plant extracts is important to promote the use of these extracts safety. Some toxic extracts may exhibit hemolytic effects on plasmatic homeostasis, renal and cardiovascular functions, and oxygen supply to organs and tissues (Carvalho et al., 2007). Certain phytochemicals, such as some saponins, flavonoids, and tannins, can alter the stability of erythrocyte membranes by interacting with the cell's plasma membrane (Sparg et al., 2004). However, different classes of saponins and flavonoids can be beneficial and non-toxic to erythrocytes, acting in the stabilization of cell membrane (Anosike et al., 2019). Thus, the concentrations of phenolic compounds and saponins found did not induce hemolysis, indicating effective protection of erythrocyte membranes and the absence of toxicity. Other Psidium species were also been reported as non-toxic to erythrocytes (Pereira et al., 2019).

The toxicity of P. oligospermum extracts to A. salina nauplii was low, except for the hexane leaf extract, which presented moderate toxicity. Similar results were found for leaf and stem extracts of P. guajava, with LC₅₀ > 100µg mL^-1 (Bautista et al., 2018; Fasola et al., 2011; Krishnaraju et al., 2006).

5. Conclusion

Leaf and stem extracts of Psidium oligospermum showed antimicrobial properties, inhibiting the growth of Gram-positive and Gram-negative bacteria and fungi, as well as antioxidant properties with low toxicity. This biological information, combined with data on chemical compounds in these extracts, indicates that Psidium oligospermum is a promising source of compounds with therapeutic properties, validating the traditional use of this species for medicinal purposes, although further research involving other evaluation techniques is needed.

Acknowledgements

The authors thank the team of the Experimental Biology Laboratory of the State University of Bahia for the contribution to this research. This research was financially supported by the Brazilian Coordination for the Improvement of Higher Education Personnel (CAPES) through a scholarship granted to the author.

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Publication Dates

• Publication in this collection
  17 Mar 2025
• Date of issue
  2025

History

• Received
  29 Sept 2024
• Accepted
  20 Jan 2025