Antibacterial Evaluation of the Rutaceae and Rosaceae Plant

Collection from Cibodas Botanical Garden, Indonesia

Intani Quarta Lailaty

, Ihsanti Fairuz Anatasya

, Agus Budiawan Naro Putra

Suluh Normasiwi

, Lily Ismaini

and Urip Perwitasari

Research Center for Applied Botany, National Research and Innovation Agency (BRIN), Cibinong, Bogor 16911, Indonesia

Faculty of Pharmacy, Universitas Gadjah Mada (UGM), Sekip Utara, Yogyakarta 55281, Indonesia

Research Center for Pharmaceutical Ingredients and Traditional Medicine, National Research and Innovation Agency

(BRIN), Cibinong, Bogor 16911, Indonesia

Research Center for Applied Microbiology, National Research and Innovation Agency (BRIN),

Cibinong, Bogor 16911, Indonesia

Keywords: Antibacterial Activity, Bioprospecting, Cibodas Botanical Gardens, Rosaceae, Rutaceae.

Abstract: Plants produce a variety of bioactive compounds with numerous biological activities, including antibacterial

properties. The potential of plant extracts possessing antibacterial properties can be further developed as raw

materials for drugs and cosmetics. In this study, antibacterial screening was conducted on three species of

plants (Rubus fraxinifolius, R. rosifolius, and Prunus cerasoides) from the Rosaceae family and two species

of plants (Acronychia pedunculata and Zanthoxylum acanthopodium) from the Rutaceae family, sourced from

the Cibodas Botanic Gardens collection in West Java. The antibacterial assay was carried out utilizing the

disc diffusion method. The bacterial isolates tested included Pseudomonas aeruginosa, Staphylococcus

aureus, and S. epidermidis. The findings demonstrated that the leaf ethanolic extract of A. pedunculata

(Rutaceae) exhibited the highest antibacterial activity compared to other species, followed by R. rosifolius

(Rosaceae). Conversely, R. fraxinifolius leaf shoot extract demonstrated the lowest antibacterial activity based

on tests against the three bacteria. Overall, all extracts produced the largest inhibition zone diameter against

S. epidermidis. Further research is necessary to develop plant bioprospecting with antibacterial properties for

pharmaceutical raw materials.

1 INTRODUCTION

Herbal medicines have been used for many

generations to treat various medical conditions,

including infectious diseases. Several natural

chemical compounds have been clinically proven to

function as medicinal raw materials, and many

studies have been conducted on their use as

antimicrobial agents (Mahady et al., 2008).

Antibiotics from natural ingredients, although

historically important, have not received the same

level of investment in research and development,

standardization, and marketing as synthetic

https://orcid.org/0000-0002-9744-9458

https://orcid.org/0000-0002-3226-3767

https://orcid.org/0000-0003-3885-0230

https://orcid.org/0000-0002-0853-183X

https://orcid.org/0000-0001-5964-4474

antibiotics. Synthetic antibacterial agents have also

been widely used in cosmetics to prevent microbial

contamination and ensure product safety (Halla et al.,

2018). Conversely, there has been a major trend

toward the application of natural resources for

therapeutic purposes. This shift is driven by consumer

concerns about the safety of synthetic ingredients and

preference for natural alternatives (Varvaresou et al.,

2009). Regulatory aspects and consumer safety

remain paramount, as evidenced by the presence of

hazardous ingredients in cosmetics in some markets

and strict laws regulating cosmetic ingredients

(Manent and Abellán, 2007).

Lailaty, I. Q., Anatasya, I. F., Putra, A. B. N., Normasiwi, S., Ismaini, L. and Perwitasari, U.

Antibacterial Evaluation of the Rutaceae and Rosaceae Plant Collection from Cibodas Botanical Garden, Indonesia.

DOI: 10.5220/0013474200004612

Paper published under CC license (CC BY-NC-ND 4.0)

In Proceedings of BRIN’s 2nd International Conference for Health Research (ICHR 2024), pages 9-18

ISBN: 978-989-758-755-9

The Rosaceae and Rutaceae plant families exhibit

significant antibacterial activity as demonstrated in

various studies. Extracts from Rosaceae fruits like

hawthorn and dog rose show potent antibacterial

properties against uropathogenic Escherichia coli

strains, reducing bacterial adhesion and biofilm

formation (Andrzej et al., 2020). Additionally, the

essential oil from rose, a member of the Rosaceae

family, exhibits antimicrobial activity against various

microorganisms, with notable effectiveness against

Staphylococcus aureus, E. coli, and Candida

albicans, showcasing its potential as a natural

antibacterial agent (Li et al., 2009). In contrast, the

ethanolic extracts from Rutaceae leaves such as

Acronychia pedunculata and Glycosmis pentaphylla,

display antibacterial effects against a range of

bacterial strains, including E. coli, S. aureus, and P.

aeruginosa, indicating their potential medicinal

applications (Hong et al., 2020).

Discovering potent antibacterial substances from

sources of nature, such as the Rutaceae and Rosaceae

plant families, holds immense promise for various

applications in healthcare and pharmaceutical

industries. These plant-derived compounds may serve

as valuable alternatives or complementary treatments

to conventional antibiotics, potentially addressing the

growing challenge of antimicrobial resistance

(Barbieri et al., 2017).

A key area of interest is the development of novel

antimicrobial therapies for treating various bacterial

infections, especially skin infections. Pseudomonas

aeruginosa InaCC B52 and Staphylococcus

epidermidis FNCC 0048 were used as gram-negative

bacteria and Staphylococcus aureus ATCC 25923

was used as gram-positive bacteria. These three

bacterias were common bacteria causing chronic skin

wound infections. The identification of potent

antibacterial compounds from Rutaceae and

Rosaceae plants could lead to the creation of new

drug candidates or the enhancement of existing

antimicrobial formulations (Chintaluri et al., 2015;

Zazharsky et al., 2020; Garcia-Oliviera et al., 2020).

These natural-based solutions may offer unique

mechanisms of action, reduced side effects, and

improved efficacy compared to synthetic antibiotics,

making them attractive options for clinicians and

patients (Fadilah et al., 2020; Mota et al., 2020).

Furthermore, the exploration of plant-derived

antibacterial agents from Rutaceae and Rosaceae

could have broader applications in the fields of food

preservation, personal care, and environmental

remediation. The antimicrobial properties of these

plant compounds could be harnessed to develop

natural preservatives for food and cosmetic products,

thereby reducing their reliance on synthetic

antimicrobials. Additionally, plant-based

antimicrobials could be explored for their potential in

water treatment and soil remediation, contributing to

more sustainable and eco-friendly solutions to

environmental challenges (van Vuuren & Viljoen,

2011; Vaou et al., 2021).

This study aimed to identify and analyze three

species of Rosaceae and two species of Rutaceae with

antibacterial activity from a collection of Cibodas

Botanic Gardens, West Java, Indonesia. Thus, it can

provide information on new antibacterial sources,

which can aid in the development of more effective

and safer medicines for treating bacterial infections

based on local natural resources. The discovery of

effective antibacterial compounds in these plant

sources could lead to the creation of new

antimicrobial medications, food preservatives, and

environmental remediation strategies, ultimately

contributing to the global efforts to combat the threat

of antimicrobial resistance.

2 METHODS

2.1 Sample Preparation

Samples from 5 plant species were acquired from

Cibodas Botanic Garden plant collections in simplisia

forms. All samples were the leaves of the plants

unless otherwise stated (fruits). They are Rubus

fraxinifolius, R. rosifolius, and Prunus cerasoides

from the Rosaceae family and Acronychia

pedunculata and Zanthoxylum acanthopodium from

the Rutaceae family. Five grams of each sample were

macerated in 70% ethanol solution at ratio of 1:5

(v/v). The sample was shaken using an incubator

shaker (Taitec BR-43FL) at 25°C, 170 rpm for 24 h.

After that, the sample was centrifuged (Tomy

KITMAN-T24) at 4°C, 5000 ×g, for 10 min to

separate the supernatant from the unsoluble

substances. Subsequently, the sample was re-

extracted twice with the same procedure and then the

filtrate was collected. Afterward, the extract was

evaporated by a rotary evaporator (IKA RV 10

Digital) to remove the solvent, followed by

lyophilization (Alpha 1-2 LD Plus Christ). The

lyophilized ethanol extract was dissolved in a 10%

dimethyl sulfoxide - phosphate-buffered saline

(DMSO-PBS) solution for antibacterial evaluation.

ICHR 2024 - BRIN’s International Conference for Health Research (ICHR)

2.2 Bacterial Isolate

The bacterial cultures used in this research were

Pseudomonas aeruginosa InaCC B52 and

Staphylococcus epidermidis FNCC 0048 as gram-

negative bacteria and Staphylococcus aureus ATCC

25923 as gram-positive bacteria. Mueller-Hinton

Agar (MHA) and Mueller-Hinton Broth (MHB)

(HiMedia, Mumbai, India) were used as culture

media and prepared according to the manufacturer's

instructions.

2.3 Antibacterial Assay

The clear zone method was employed for a semi-

quantitative antibacterial activity test. The suspension

of each bacterial isolate of P. aeruginosa, S. aureus,

or S. epidermidis was poured and spread on Mueller-

Hinton Agar (MHA) in petri dishes. A 0.5 cm

diameter Whatman filter paper (paper disk) was then

positioned on the agar plate, followed by adding 10

μL of sample (lyophilized ethanol extract dissolved in

10% DMSO-PBS) onto the paper disk. Each sample

was prepared at a concentration of 1000 µg/mL.

Additionally, the positive and negative controls used

were 12.5 µg/mL of commercial chloramphenicol

(Novapharin, Gresik, Indonesia) and 10% DMSO-

PBS, respectively. After incubating bacterial cultures

at 37°C for 24 hours, the zone of inhibition diameter

was measured using a caliper. Triplication was

performed for each sample tested. The inhibition

zones formed in each test were observed and

measured as the appearance of antibacterial activity.

2.4 Data Analysis

The statistical significance of the difference was

tested by the one-way ANOVA method completed by

the Tukey-Kramer test. Values with *p < 0.05 or

**p < 0.01 were considered statistically significant

against negative control (10% DMSO-PBS). In

addition, plant descriptions were explained by works

of literature. Plant origin was based on the Cibodas

Botanic Gardens data collection database, plant

distribution by POWO database, and antibacterial

compounds were collected from related journal

articles.

3 RESULTS AND DISCUSSION

3.1 Plant Characteristics of Rutaceae

and Rosaceae

The Rutaceae and Rosaceae families are well-known

for their diverse and often economically important

plant species. The Rutaceae family, commonly

known as the rue or citrus family, encompasses

various plants, including familiar citrus fruits, such as

oranges, lemons, and limes. These plants are

renowned for their aromatic compounds and have

long been used in traditional medicine because of

their medicinal properties. On the other hand, often

called the "rose family", the Rosaceae family is a

broad group of plants that includes a range of fruits,

including strawberries, pears, and apples, as well as

ornamental species like roses. Like the Rutaceae

family, Rosaceae plants have a rich history of

traditional medicinal use, with many species

exhibiting a range of bioactivities, including

antimicrobial properties. Plant descriptions with

antibacterial properties from Rutaceae and Rosaceae

species from the Cibodas Botanic Gardens collection

were described in Table 1.

Approximately 1800 species and 156 genera belong

to the Rutaceae family, which is widely distributed

throughout tropical and subtropical climates, especially

Southeast Asia. Many species of Rutaceae, such as A.

pedunculata and Z. acanthopodium, have many

biologically active compounds. Numerous beneficial

goods, including medicines, food, spices, and essential

oils, are made from those natural resources (Van et al.,

2020).

Often referred to as claw-flowered Laural or Lake,

Kayu Semidra, or Jejerukan (in Indonesia), Acronychia

pedunculata L. (Rutaceae) is a tiny tree with glabrous

branches and pale, smooth bark. This plant's leaves are

oval, 7.5-12.5 cm long, and can be placed simply,

oppositely, or alternately. The flowers are arranged

loosely in pyramidal or divaricate patterns on long,

straight axillary peduncles and are small, regular,

polygamous, and pale yellowish green in color.

Usually, flowering takes place from February to April.

The spherical, indehiscent fruits measure between 1.2

and 1.8 centimeters in length. It's interesting to note

that fruits have four chambers, with one seed in each

chamber (Jayaweera, 1982). One species of the

Rutaceae family that is widespread in Indonesia is A.

pedunculata (Figure 1a). Traditional medicine has

utilized stem bark to treat rheumatism, diarrhea, fever,

and asthma (Tanjung et al., 2018).

Antibacterial Evaluation of the Rutaceae and Rosaceae Plant Collection from Cibodas Botanical Garden, Indonesia

Table 1: Plant descriptions with antibacterial properties.

Scientific

names

Family Origin* Distribution** Antibacterial activity Compounds References

Rubus

fraxinifolius

Poir.

Rosaceae West

Java

Lesser Sunda Is.,

Taiwan,

Mauritius,

Rodrigues,

Réunion

Leaf extract from R.

fraxinifolius had

antibacterial potency

against B. subtilis, S.

aureus, and

. coli

Flavonoids,

quercetin,

naringenin

Dewi et al.

(2019)

Rubus rosifolius

Sm.

Rosaceae West

Java

Central & S.

China to Tropical

Asia

The fruit crude extract

of R. rosifolius had

antimicrobial activity

against a wide range of

microorganisms,

including S. aureus and

. coli

The phenolic

compounds,

alkaloids,

anthraquinones,

and alcohols

Alvares et

al. (2013)

Prunus

cerasoides

Buch.-Ham. ex

D.Don

Rosaceae Himalaya NE. Pakistan to

Indo-China

Assam, Myanmar,

East Himalaya,

Pakistan, Laos,

Nepal, Vietnam,

Sri Lanka, West

Himalaya,

Thailan

Ethyl acetate stem bark

extract P. cerasoides

inhibits the growth of

Staphylococcus

aureus and Klebsiella

pneumoniae

Phytoconstituent

, flavonoids,

diterpenes, and

cardiac

glycosides

Mahajan &

Arora (2019)

Acronychia

pedunculata

(L.) Miq.

Rutaceae Java Tropical &

Subtropical Asia

Methanol extract from

a root, seed, flower,

leaves, and stem bark

extract gave the

maximum inhibition on

test pathogenic bacteria

(S. typhi, E. coli, B.

subtilis, and S. aureus).

It has been

demonstrated that the

essential oil extracted

from the plant's aerial

parts has a wide range

of antibacterial activity

against different

microorganisms.,

particularly

Staphylococcus

epidermidis and

Salmonella enterica

Sterols,

flavonoids,

terpenoids,

resins, saponins,

carbohydrates,

tannins, and

glycosides

Lesueur et al.

(2008),

Gireesha &

Raju (2016),

Ratnasooriya

et al. (2016),

Muthukuda

& Jayakody

(2021)

Zanthoxylum

acanthopodium

DC.

Rutaceae North

Sumatera

Himalaya to S.

China and W.

Malesia

The antibacterial

activity of the

Andaliman fruit's ethyl

acetate extract was

stronger response S.

aureus and S.

typhimurium than E.

Coli. 50 - 75% extracts

fruits also against

Salmonella typhi,

although did not against

all aquaculture

atho

ens

Alkaloids,

steroids, tannins

and saponins

Muzafri et al.

(2018),

Sihombing et

al. (2019),

Sibero et al.

(2021), Adrian

et al. (2023)

In North Sumatera Utara, Indonesia, andaliman (Zanthoxylum acanthopodium DC.) is a common wild plant.

Many members of the Batak ethnic group use Andaliman for food processing, particularly fish and meat. It is

known as "Batak pepper" for its hot flavor and peculiar scent. Andaliman is used by the Batak population as a

traditional medicine in addition to being used in food preparation (Adrian et al., 2023).

ICHR 2024 - BRIN’s International Conference for Health Research (ICHR)

Figure 1: a) A. pedunculata, b) Z. acanthopodium.

Figure 2: a) R. fraxinifolius, b) R. rosifolius, and c) P. cerasoides.

With low, prickly branches, trunks, and twigs, the

Andaliman is a shrub or small tree that can grow up

to 6 meters in height. Its odd-pinnate, dispersed,

stemmed compound leaves, which are 5–20 cm long

and 3–15 cm broad, contain oil glands. Three to

eleven thorny, oblong-shaped leaflets with tapering

ends and coarsely serrated edges, reaching 1 to 7 cm

in length and 0.5 to 2.0 cm in width, are affixed to the

winged rachis. Some leaves have a green top surface

and a reddish-green underside, while young or light

leaves have a sparkling green top surface and a green

bottom. The petals are pale yellow, androgynous, and

measure 5-7 cm long (1-2 cm). The flower has three

to four pistils, an apocarpous ovule, reddish anthers,

and around five to six stamens at the base. Andaliman

produces actual box fruits or capsules that are round,

2-3 mm in diameter, shiny black, contain one seed,

have a hard skin, and are brilliant green when young

or dark red when old. After ten days at room

temperature, the black seeds will sprout from the old

fruit (Rahmawaty et al., 2019; Sonangda et al., 2019).

The Andaliman plant is presented in Figure 1b.

Genus Rubus belongs to the Rosaceae family,

Rosoideae subfamily. With more than 1,350 species,

it is a sizable and varied genus. In high-altitude

woods, such as those in the Himalayas and the

Nilgiris, rubus is extensively distributed (Schulz and

Chim, 2019; Sharma et al., 2021). The ragimot berry

(Rubus spp.) is an erect shrub that grows to a height

of 2-3 meters and has stems with up to 6 mm prickles.

Its pinnate leaves have a terminal leaflet and four

pairs of opposing leaflets. These elliptic leaflets are

2-9 × 1.4 cm, with 7-10(-15) vein pairs, scant hair

coating, and serrated edges (Lamb, 2019). Grayish

yellow-green flowers with bulging shapes grow on

inflorescence panicles that measure 6-20 cm long

(Normasiwi et al., 2021).

R. rosifolius J. Sm. and Rubus fraxinifolius Poir.

are Indonesian Raspberry species native to Indonesia

(Figure 2a dan 2b). In West Java (Sundanese), the

fruit of R. rosifolius and R. fraxinifolius is known as

"Beberetean" or "Arben". Both fruits are edible, have

a similar appearance (small, red), and possess a sweet

instead of sour taste (Desmiaty et al., 2018).

Prunus is a member of the Rosaceae, specifically

the Amygdalaceae subfamily. It consists of around

430 deciduous and evergreen shrub and tree species

that are mostly found in the northern hemisphere and

Antibacterial Evaluation of the Rutaceae and Rosaceae Plant Collection from Cibodas Botanical Garden, Indonesia

temperate zones (Agrawal et al., 2024). Prunus has

simple, alternate, generally lanceolate, unlobed

leaves with nectarines on the stem. These flowers

have five petals, five sepals, and many stamens. They

are often white to pink but can also be crimson.

Flowers bloom singly, in umbels of two to six, or

even more, on racemes. Fruits are fleshy drupes with

a single rather big, hard-coated seed, popularly called

the stone fruit (Joseph et al., 2018). In India, Prunus

grows widely, and the majority of them have

significant therapeutic and commercial value, one of

which is P. cerasoides or Himalayan Cherry Blossom

(Agrawal et al., 2024), see Figure 2.

3.1 Antibacterial Activity

The diameter of the inhibition zones against different

bacteria was used to measure the antibacterial activity

of ethanolic extracts from the leaves and fruits of

Rosaceae and Rutaceae species (see Figure 3, 4, and

5). The ethanol extracts of the leaves of R. rosifolius,

A. pedunculata, and R. fraxinifolius (young leaves)

were considered as the top three that significantly

inhibited the growth of all three bacterial strains, i.e:

P. aeruginosa, S. aureus, and S. epidermidis.

However, results revealed that ethanol extract of A.

pedunculata leaves (from the Rutaceae family)

exhibited the highest antibacterial activity compared

to other species, followed by R. rosifolius (Rosaceae).

Conversely, R. fraxinifolius (p) leaf bud extract

demonstrated the lowest antibacterial activity based

on tests against the three bacteria. Overall, all extracts

produced the largest inhibition zone diameter against

S. epidermidis.

Figure 3: Antibacterial activity of plant collections from the families of Rutaceae and Rosaceae against Pseudomonas

aeruginosa. Values with *p < 0.05 or **p < 0.01 were considered statistically significant against negative control (10%

DMSO-PBS). Data were represented as mean ± SD. All samples were the leaves of the plants unless otherwise stated (fruits).

Notes: p: leaf bud, dm: young leaf.

Figure 4: Antibacterial activity of plant collections from the families of Rutaceae and Rosaceae against Staphylococcus

aureus. Values with *p < 0.05 or **p < 0.01 were considered statistically significant against negative control (10% DMSO-

PBS). Data were represented as mean ± SD. All samples were the leaves of the plants unless otherwise stated (fruits). Notes:

p: leaf bud, dm: young leaf.

ICHR 2024 - BRIN’s International Conference for Health Research (ICHR)

Figure 5: Antibacterial activity of plant collections from the families of Rutaceae and Rosaceae against Staphylococcus

epidermidis FNCC 0048. Values with *p < 0.05 or **p < 0.01 were considered statistically significant against negative control

(10% DMSO-PBS). Data were represented as mean ± SD. All samples were the leaves of the plants unless otherwise stated

(fruits). Notes: p: leaf bud, dm: young leaf.

The once-considered harmless bacterium S.

epidermidis, which thrives on human skin, has

developed into a significant opportunistic pathogen.

Numerous infections have been linked to these

bacteria, and treatment has been impeded by its

resistance to several drugs. New strains of multidrug-

resistant bacteria may arise as a result of S.

epidermidis acting as a reservoir for antibiotic

resistance genes that can be passed from one

Staphylococci species to another, including S. aureus

(Ahmadunissah et al., 2022).

In this study, A. pedunculata had the highest

antibacterial activity against the three test bacteria.

This is in line with the research of Van et al. (2020)

that all six bacterial strains—Bacillus cereus,

Staphylococcus aureus, Escherichia coli,

Pseudomonas aeruginosa, Salmonella enteritidis,

and Salmonella typhimurium—were able to

withstand the ethanolic extracts made from A.

pedunculata leaves.

Further, the extract of Acronychia pedunculata

contained polyphenols, triterpene alcohols, and

acetophenones, which were effective in inhibiting the

activity of Staphylococcus epidermidis and

Salmonella enterica (Kumar et al., 1989; Su et al.,

2003).

In addition, as shown in Figure 3, 4, and 5, the

ethanol extract of the fruit of Z. acanthopodium

slightly exhibited a wider inhibition zone compared

to that of its leaf ethanol extract. Majumder et al.

(2014) reported that traditionally the fruits of

Andaliman have been used as a spice, to treat fish

poisoning, to alleviate toothaches, and to treat

stomach colic, etc. The essential oil analysis of

Andaliman fruit identified 21 components, with

major components i.e. δ-3-carene (13.525%),

Limonine (16.903%), Eucalyptol (36.563%), and

Methyl-cinnamate (9.366%). With a broader zone of

inhibition, andaliman exhibits encouraging

antibacterial action, particularly against S. aureus.

Furthermore, the ethanol extract of the young leaf

of R. fraxinifolius showed higher antibacterial activity

than that of its leaf bud. Based on Shamsudin et al.

(2019), In addition to other phytochemicals including

alkaloids, phytosterols, tannins, and terpenoids, R.

fraxinifolius has been shown to possess flavonoids

and phenolic compounds. Free radical-related

illnesses have been treated and prevented with these

chemical substances. These substances exhibit

promise for use as natural antioxidants for human

well-being.

4 CONCLUSIONS

Natural materials have become increasingly popular

as traditional remedies in Indonesia. Traditional

treatments have been reported to have fewer negative

effects than chemical-based therapies. Many plant

species are widely used by the community as

traditional medicinal ingredients in daily life and have

antibacterial properties. Hence, according to our

results, plants from the Rutaceae and Rosaceae

families, especially the ethanol extracts of the leaves

of R. rosifolius (Indonesian Raspberry) and A.

pedunculata (Kayu Semidra) have the potential to be

further utilized as an active ingredient for

antibacterial products, especially against skin bacteria

Antibacterial Evaluation of the Rutaceae and Rosaceae Plant Collection from Cibodas Botanical Garden, Indonesia

(Pseudomonas aeruginosa, Staphylococcus aureus,

and S. epidermidis) which are safer and more

comfortable. However, a more specific antibacterial

mechanism needs further investigation.

ACKNOWLEDGEMENTS

This study was supported by the Indonesian Institute

of Sciences (LIPI) through “Program Prioritas

Nasional Gelombang Ke-2 di Lingkungan Deputi

Bidang Ilmu Pengetahuan Teknik LIPI” Year 2021.

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