Antibacterial activity in secondary metabolite extracts of heterotrophic bacteria against&nbsp;<i>Vibrio alginolyticus, Aeromonas hydrophila,</i>&nbsp;and&nbsp;<i>Pseudomonas aeruginosa</i>

Jarod Setiaji; Feli Feliatra; Hilwan Yuda Teruna; Iesje Lukistyowati; Indra Suharman; Zainal Abidin Muchlisin; Teuku Iskandar Johan

doi:10.12688/f1000research.26215.1

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Research Article

Antibacterial activity in secondary metabolite extracts of heterotrophic bacteria against Vibrio alginolyticus, Aeromonas hydrophila, and Pseudomonas aeruginosa

[version 1; peer review: 2 approved]

Jarod Setiaji^1,2, Feli Feliatra ¹, Hilwan Yuda Teruna³, [...] Iesje Lukistyowati¹, Indra Suharman¹, Zainal Abidin Muchlisin⁴, Teuku Iskandar Johan²

Jarod Setiaji^1,2, Feli Feliatra ¹, [...] Hilwan Yuda Teruna³, Iesje Lukistyowati¹, Indra Suharman¹, Zainal Abidin Muchlisin⁴, Teuku Iskandar Johan²

PUBLISHED 21 Dec 2020

Author details Author details

¹ Faculty of Fisheries and Marine Science., Universitas Riau, Pekanbaru, Riau, Indonesia
² Faculty of Agriculture, Universitas Islam Riau, Pekanbaru, Riau, Indonesia
³ Faculty of Mathematics and Natural Science, Universitas Riau, Pekanbaru, Riau, Indonesia
⁴ Faculty of Marine and Fisheries, Universitas Syiah Kuala, Banda Aceh, Aceh, 23111, Indonesia

Jarod Setiaji
Roles: Conceptualization, Data Curation, Formal Analysis, Funding Acquisition, Investigation, Writing – Original Draft Preparation

Feli Feliatra
Roles: Conceptualization, Methodology, Project Administration, Supervision, Validation, Writing – Review & Editing

Hilwan Yuda Teruna
Roles: Methodology, Resources, Software, Supervision, Visualization, Writing – Original Draft Preparation

Iesje Lukistyowati
Roles: Methodology, Supervision, Validation, Writing – Original Draft Preparation

Indra Suharman
Roles: Methodology, Software, Supervision, Validation, Visualization

Zainal Abidin Muchlisin
Roles: Supervision, Validation, Visualization, Writing – Review & Editing

Teuku Iskandar Johan
Roles: Formal Analysis, Investigation, Methodology, Resources, Software

OPEN PEER REVIEW

REVIEWER STATUS

Abstract

Background: Disease causing bacteria such as Vibrio alginolyticus, Aeromonas hydrophila, and Pseudomonas aeruginosa present a problem for fish farming. Treatment to remove them are generally carried out using antibiotics which have side effects on fish, the environment and humans. However, the use of antibacterial compounds derived from heterotrophic bacteria serve as a good alternative for antibiotics. Therefore, this study aimed to explore antibacterial activity in the secondary metabolite extracts of heterotrophic bacteria against Vibrio alginolyticus, Aeromonas hydrophila, and Pseudomonas aeruginosa.
Methods: Heterotrophic bacteria namely Bacillus sp. JS04 MT102913.1, Bacillus toyonensis JS08 MT102920.1, Bacillus cereus JS10 MT102922.1, Bacillus sp. JS11 MT102923.1, Pseudoalteromonas sp. JS19 MT102924.1, Bacillus cereus JS22 MT102926.1, and Bacillus sp. strain JS25 MT102927.1 were used in this study. The sequences of these bacteria have been deposited and are available from NCBI GenBank. Each heterotrophic bacterium was cultured on 6L nutrient broth for 8 days, and extracts produced using ethyl acetate to obtain their secondary metabolites. These extracts were tested for their phytochemical contents using FT-IR and also tested for their inhibitory property in pathogenic bacteria by agar diffusion method.
Results: Phytochemical test results showed that the seven heterotrophic bacterial isolates produced terpenoid compounds. Based on the inhibitory test, the secondary metabolite extracts from Bacillus sp strain JS04 had the highest inhibitory effect on the growth of pathogenic bacteria namely, V. alginolyticus (17.5 mm), A. hydrophila (16.8 mm), and P. aeruginosa (17.3 mm).
Conclusion: It was concluded that the secondary metabolite extracts of heterotrophic bacteria inhibit the growth of V. alginolyticus, A. hydrophila, and P. aeruginosa.

Keywords

antibacterial, fish pathogens, heterotrophic bacteria, secondary metabolites

Corresponding author: Feli Feliatra

Competing interests: No competing interests were disclosed.

Grant information: The author(s) declared that no grants were involved in supporting this work.

Copyright: © 2020 Setiaji J et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

How to cite: Setiaji J, Feliatra F, Teruna HY et al. Antibacterial activity in secondary metabolite extracts of heterotrophic bacteria against Vibrio alginolyticus, Aeromonas hydrophila, and Pseudomonas aeruginosa [version 1; peer review: 2 approved]. F1000Research 2020, 9:1491 (https://doi.org/10.12688/f1000research.26215.1) First published: 21 Dec 2020, 9:1491 (https://doi.org/10.12688/f1000research.26215.1) Latest published: 21 Dec 2020, 9:1491 (https://doi.org/10.12688/f1000research.26215.1)

Introduction

Bacteria diseases in fish stocks constitute a major problem for fish farming, since they cause significant economic losses^1–3. Common pathogenic bacteria that affect fish include Vibrio alginolyticus, Aeromonas hydrophila and Pseudomonas aeruginosa^4–9. V. alginolyticus is a gram-negative bacteria which is an opportunistic pathogen in marine animals^10–13. Bacterial diseases cause different fish infections such as, exophthalmia, ulcers, septicemia, and corneal damage^14–16. Aeromonas hydrophila is found to be the main cause of the septicemia epidemic in freshwater fish^17,18. Its outbreak causes tissue damage of the spleen, gills, and the fish's stomach¹⁹. A. hydrophila is found to frequently infect various fish species namely, catfish (Ictalurus punctatus)²⁰, carp (Cyprinus carpio) and catfish (Pangasius hypophthalmus)²¹, tilapia (Oreochromis niloticus)²², salmon (Oncorhynchus masou masou)²³, snapper (Lates calcarifer)²⁴, striped snakehead (Channa striata)²⁵, cod (Gadus macrocephalus), and tank goby (Glossogobius guris)²⁶. Meanwhile, P. aeruginosa is found to infect freshwater and marine fish^27,28, with infection being characterized by the expression of red spots due to bleeding, skin darkens, loose scales, protruding eyes, fin erosion²⁹, behavioural changes due to disruption of locomotor activity³⁰, and abnormal swimming³¹.

Bacteria disease treatment is generally carried out using antibiotics, however, these can have adverse effects on the fish and their environment^32–37. The accumulation of antibiotics in the fish increase the risk of bacterial resistance^38,39. Escherichia coli bacteria isolated from the digestive organs of catfish showed high resistance levels towards tetracycline, ampicillin, and chloramphenicol⁴⁰. Therefore, it is necessary to explore natural compounds with antibacterial activity⁴¹. Sea water is a potential source of heterotrophic bacteria that produce antimicrobial compound⁴², and have probiotic activity⁴³

Sea bacteria such as, Bacillus sp. B. cereus, B. toyonensis, and Pseudoalteromonas sp., are known to inhibit the growth of pathogenic bacteria namely, V. alginolyticus, A. hydrophila, and Pseudomonas sp⁴³. They also produce antimicrobial compounds such as, Pseudoalteromonas⁴⁴. Pseudoalteromonas piscicida produces antimicrobial substances that inhibit the growth of different pathogenic bacteria namely, Vibrio vulniosis⁴⁵, Bacillus sp⁴⁶, B. pumilus⁴⁷, and B. subtilis^48,49. Bacillus amyloliquefaciens shows antibacterial activity towards pathogenic bacteria such as, Aeromonas hydrophila, Vibrio harveyi, V. vulnificus, and V. parahaemolyticus⁵⁰. Meanwhile, Bacillus subtilis shows antibacterial activity towards the pathogens Vibrio parahaemolyticus, V. vulnificus, and Aeromonas hydrophila⁵¹.

Heterotrophic bacteria extracted from Riau sea waters were examined and found to able to inhibit the activity of pathogenic bacteria Aeromonas salmonicida, Edwarsiela tarda and Edwarsiela ictaluri as previously reported by Setiaji et al.⁵². However, the antibacterial activity of these heterotrophic bacteria extracted from Riau sea waters on the pathogenic bacterial namely, Vibrio alginolyticus, Aeromonas hydrophila, and Pseudomonas aeruginos have never been examined for its potential against pathogenic bacteria. Therefore, this study aims to explore antibacterial activity in secondary metabolite extracts of heterotrophic bacteria isolated from Riau sea water, against pathogenic bacteria namely, V. alginolyticus, A. hydrophila, and P. aeruginosa.

Methods

Bacterial culture

The heterotrophic bacteria isolates were collected from sea waters in Sungai Pakning Bengkalis Regency Riau Province Indonesia (North latitude 01^o21’36,8” and East longitude 102^o09’34,1”). 1 liter of the sea water was collected at 50 cm depth by using a water sampler (Tiolan Lab, type: WSV-BIT22), then was transferred into a sample bottle and was put into a coolbox filled with ice at 15°C, before being transported by car for 1 hour to the laboratory. The heterotrophic bacteria was cultured using nutrient Agar (NA; Merck-1.05450.0500). The heterotrophic bacteria cultured were used for an antagonist test against pathogen bacteria. The antagonist test procedure is as follows, 1 ml of pathogenic inoculants (OD _600nm = 0.08–0.1) (OD measured with Thermo scientific, Genesys 10S UV-Vis) was added to 15 ml liquid nutrient Agar media at 50ºC, then homogenized, and poured into a petri dish to solidify. Furthermore, Oxytetracycline antibiotic disc paper (Oxoid, CT0041B, OT30 mcg) was used as the positive control, while 30 µl aquades (Kimiapedia id-1720602804) was dripped to a disc paper (Macherey-nagel, MN827 ATD) as the negative control. 30 µl heterotrophic bacterial isolate taken from bacteria culture in nutrient Broth (NB; Merck-1.05443.0500) was dripped to a disc paper and incubated at 30°C for 24 hours. The inhibitory power of heterotrophic bacterial isolate was measured from the diameter of clear zone formed around the disc. From the antagonist test, eight isolates with the best inhibition were collected, and the heterotrophic bacteria was identified using 16S rDNA technique⁴³. The sequenced products were run through BLAST (NCBI Basic Local Alignment Search Tool) and registered to GenBank.

The pathogenic bacteria were obtained from the collection at the Marine Microbiology Laboratory of the Faculty of Fisheries and Marine Science, University of Riau, Indonesia. The heterotrophic and pathogenic bacteria were cultured on the nutrient Agar (NA; Merck-1.05450.0500). The cultured medium was sterilized in an autoclave at a pressure of 15 psi and 121°C for 15 minutes. After 1 hour at room temperature, the medium was inoculated by the heterotrophic bacteria and the pathogenic bacteria. Then the bacteria were incubated in an incubator (Memmert, Model 30–1060) at 30°C for 24 hours.

Isolates test

Previous studies showed that eight heterotrophic bacterial isolates possessed the potential to produce pathogens. Seven of these species were used in this study namely, Bacillus sp. JS04 MT102913.1, Bacillus toyonensis JS08 MT102920.1, Bacillus cereus JS10 MT102922.1, Bacillus sp. JS11 MT102923.1, Pseudoalteromonas sp. JS19 MT102924.1, Bacillus cereus JS22 MT102926.1 and Bacillus sp. strain JS25 MT102927.1 have been deposited in GenBank.

Then, each bacterium was cultured in a 6 L nutrient Broth (NB; Merck-1.05443.0500) diluted with sea water of salinity 29 ppt and aerated for 8 days. After this, the bacteria were mixed with ethyl acetate (P.a) at ratio 1:1 and shaken vigorously to homogenize. Subsequent filtering was performed until a clear filtrate was obtained using funnel and filter paper (Whatman 41, no. 1441–125), and evaporated with a rotary evaporator (Cole Parmer, N-1300) at 50°C and a speed of 50 rpm. This allowed thick secondary metabolite extracts to be obtained⁵³.

Phytochemical test and Fourier-transform infrared spectroscopy (FT-IR)

Phytochemical test was conducted on the secondary metabolite extracts of heterotrophic bacteria, which included tests for alkaloid, terpenoid, flavonoid, phenolic, and saponin compounds⁵⁴.

Mayer reagent was prepared by adding 1.36 g HgCl₂ (Merck, 1.04419. 0050) to 60 mL distillled water and 5 g Ki (Meck 1.05043.1000) to 10 mL distilled water. Both solutions were then mixed with a further 20 mL distilled water. The Liebermen – burchad reagent was prepared by mixing 97% H₂SO₄ (Merck 1.00731.2500) and 100% CH₃COOH (Merck 1.00063.2500).

Alkaloids were tested for using using 10 mg heterotrophic bacteria extract and 250 µL Mayer reagent.

The terpenoid was tested using 10 mg heterotrophic bacteria extract, 10 drops of CH₃COOH, and 3 drops of H₂SO₄.

Flavonoid tests were performed using 10 mg heterotrophic bacteria extract added to 5 mL distilled water. This was then boiled before adding 0.05 g Mg (Merck 1.05815.1000) and 10 drops of 37% HCl (Merck 1.00317. 2500), the mixture was then shaken for one minute.

Phenolic compounds were tested by using 10 mg heterotrophic bacteria extract combined with 500 µL 5% FeCl₃ (Merck 1.03943.0250).

Saponin compounds were tested for using 10 mg heterotrophic bacteria extract added to 5 mL distilled water which was then shaken for 1 minute. 150 µL 1N HCl (Merck 1.00317. 2500) was then added, and shaken for another minute.

A positive alkaloid test was indicated by the formation of a white precipitate after adding Mayer regent. A positive terpenoid test was indicated by the formation of a red colour. A positive flavonoid test was indicated by a red colour change. Phenolic compounds were indicated by a blue colour change. Saponin compounds were indicated by a foam forming.

Meanwhile, to determine the functional groups in secondary metabolite extracts, FT-IR (Shimadzu, IR prestige-21, IR solution software ver. 1.1) spectroscopy analysis was performed. This was conducted by crushing 1 mg of each extract, added to KBr (Merck-1.04950.0500), and mixed vigorously until homogenized. This mixture was then measured for infrared absorbance at 4500–450 cm wavelength.

Inhibitory activity of heterotrophic bacterial extract

The secondary metabolite extracts of heterotrophic bacteria obtained were tested on pathogenic bacteria namely, V. algynolyticus, A. hydrophila, and P. aeruginosa using agar diffusion method, and 6 mm disc paper (Macherey-nagel, MN827 ATD)⁵⁵. The procedure is as follows, 1 ml of pathogenic inoculants (OD _600nm = 0.08–0.1) (OD measured with Thermo scientific, Genesys 10S UV-Vis) added to 15 ml liquid nutrient agar media at 50°C, then homogenized, and poured into a petri dish to solidify. Furthermore, Oxytetracycline antibiotic disc paper (Oxoid, CT0041B, OT30 mcg) was used as the positive control, while methanol disc paper was the negative control. The metabolite extracts were then dissolved in 1 mg / mL methanol (P.a) and incubated at 30°C for 24 hours. The inhibitory power of heterotrophic bacterial extracts was measured from the diameter of clear zone formed around the disc.

Data analysis

The data were subjected to one-way analysis of variance followed by the Post Hoc Tukey multiple range test using R 4.0 software (GNU General Public License), p<0.05 is considered to indicate a statistically significant difference.

Results

Phytochemical test and functional groups

Phytochemical test results of the metabolite extracts when added to Lieberman-Burchard reagents produced a red colour indicating the presence of terpenoids in the seven isolates. Meanwhile, the test for alkaloid, flavonoid, phenolic, and saponin compounds gave negative results.

Based on infrared spectrum analysis, the secondary metabolite extracts of Bacillus sp. strain JS04 contained O-H alcohol, C-H aldehyde, O-H carboxylic acid, and C=C alkene groups. Bacillus toyonensis JS08 contained C-H alkanes, C=N nitriles, C=O carbonyl, and C-N amine groups. Bacillus cereus JS10 contained C-H alkanes, O-H carboxylic acid, C=C alkenes, and C-H alkanes groups. Bacillus sp. JS11 contained O-H alcohol, C-H alkanes, O-H carboxylic acids, and C=O carbonyl groups. Pseudoalteromonas sp. JS19 contained alcohol O-H, C-H alkanes, C=O carbonyl, and C=C alkenes groups. Bacillus cereus JS22 contain O-H alcohol, C-H alkane, C=O carbonyl, and C=C alkene groups. Bacillus sp. JS25 contain C-H alkanes, O-H carboxylic acids, O-H alcohols, and C=C alkenes groups (Table 1⁵⁶).

Table 1. Infrared spectrum of secondary metabolite extracts of heterotrophic bacteria.

Secondary metabolite extracts	Spectrum (cm^-1)	Functional groups
Bacillus sp. strain JS04	3148 2732 2535 827	O-H C-H O-H C=C
Bacillus toyonensis strain JS08	2925 2361 1722 1229	C-H C=N C=O C-N
Bacillus cereus strain JS10	2925 2735 1669 1459	C-H O-H C=C C-H
Bacillus sp. strain JS11	3330 2925 2527 1721	O-H C-H O-H C=O
Pseudoalteromonas sp. strain JS19	2930 2732 1720 1455	C-H O-H C=O C-H
Bacillus cereus strain JS22	3567 2925 1710 827	O-H C-H C=O C=C
Bacillus sp. strain JS25	2895 2602 1364 830	C-H O-H O-H C=C

Inhibitory activity

The results showed that the seven heterotrophic bacterial isolates inhibited the growth of pathogenic bacteria. The extracts inhibitory activity against pathogenic bacteria are shown in Table 2⁵⁶. The average inhibition zone diameter of the extracts against pathogenic bacteria namely, V. alginolyticus, A. hydrophila, and P. aeruginosa ranges from 9.3 to 17.5 mm, 9.3 to 16.8 mm, and 8.5 to 17.3 mm, respectively. This inhibitory zone activity was indicated by the presence of clear zones formed around the disc paper. The largest inhibition zone diameter of the extracts against the growth of pathogenic bacteria was derived from isolates of Bacillus sp. strain JS04 (17.5 mm) on V. alginolyticus, 17.3 mm on P. aeruginosa, and 16.8 mm on A. hydrophila.

Table 2. Inhibitory activity in the secondary metabolite extracts of heterotrophic bacteria against pathogenic bacteria.

Mean values with different superscripts in the same columns were significantly different (p < 0.05).

Secondary metabolite extracts	Average of inhibition zone diameter (mm)
Secondary metabolite extracts	V. alginolyticus	A. hydrophila	P. aeruginosa
Bacillus sp. strain JS04	17.5^a	16.8^a	17.3^a
Bacillus toyonensis strain JS08	11.0^b	9.5^b	10.0^b
Bacillus cereus strain JS10	10.8^b	8.5^b	9.5^b
Bacillus sp. strain JS11	10.8^b	9.0^b	9.5^b
Pseudoalteromonas sp. strain JS19	10.8^b	9.8^b	9.8^b
Bacillus cereus strain JS22	9.3^b	9.3^b	8.5^b
Bacillus sp. strain JS25	15.8^a	15.5^a	16.3^a

Discussion

Phytochemical test results showed that the seven heterotrophic bacterial isolates produced terpenoids, which consist 5 carbon atoms or isoprene (C5) units. Microbes carry out biosynthesis by producing isopentyl pyrophosphate and dimethyl allyl pyrophosphate for terpenoid formation⁵⁷. A significant relationship between terpenoids gene expression and isoprene production in Bacillus subtilis has previously been reported⁵⁸.

Infrared spectrum analysis provided information about the detected compounds in the mixture⁵⁹. Metabolite extracts showed the presence of hydroxyl, aldehyde, carboxylic acid, alkene, alkane, carbonyl, and amine functional groups in these extracts. This indicated that the seven bacterial isolates produced terpenoids, while the functional groups contained in the terpenoids were namely, O-H hydroxyl, C-H aliphatic, carbonyl, C-H cyclic, and carboxylic acid⁶⁰.

The result of inhibitory activity in the secondary metabolite extracts of Bacillus sp. strain JS04 showed the largest inhibition zone against the growth of pathogenic bacteria. The formation of clear zones on culture media indicated that heterotrophic bacteria produced terpenoid compounds for antibacterial purposes.

The terpenoid compounds contained several phytochemicals that possess antimicrobial activity⁶¹. For example, Terpenes and terpenoids have been reported to exert antimicrobial activity against a wide variety of bacteria, both Gram-positive and Gram-negative⁶². Terpenes cause membrane disruption through acting on lipophilic compound in the membrane⁶³. Therefore, terpenoid compounds were able to prevent the forming of biofilm cell in the bacterium Streptococcus mutans^60,64.

There are many antimicrobial compounds produced by sea bacteria especially from the Bacillus and Pseudoaltreromonas genus. For instance, B. pumilus produces antimicrobial compound against V. algynolyticus, V. anguillarum, Listeria monocytogenes and Staphylococcus aureus pathogens⁴⁸. The Bacillus sp. from sea water produced chemical compound effective at preventing motility of V. Algynolyticus⁴⁷. Bacillus subtilis produced antibacterial compound against Aeromonas hydrophila and Vibrio parahemolyticus pathogens⁴⁹. The genus Pseudoalteromonas hosts 16 antimicrobial metabolite producers. To date, a total of 69 antimicrobial compounds are classified into alkaloids, polyketides, and peptides⁴⁵. Furthermore, the bacterium Pseudoalteromonas rubra which was symbiotic with soft coral Sarcophyton sp. produced carotenoid pigments with antibacterial activity against Staphylococcus aureus⁶⁵ and V. algynolyticus pathogens⁶⁶.

Conclusion

The secondary metabolite extracts produced by the seven isolates of haterotrophic bacteria can inhibit the growth of pathogenic bacteria, namely V. alginolyticus, A. hydrophila, and P. aeruginosa. The secondary metabolite extracts of Bacillus sp. strain JS04 has the highest inhibitory activity against the growth of these three pathogenic bacteria.

Data availability

Underlying data

Figshare: Antibacterial activity in secondary metabolite extracts of heterotrophic bacteria against Vibrio alginolyticus, Aeromonas hydrophila, and Pseudomonas aeruginosad Item. https://doi.org/10.6084/m9.figshare.12818798.v3⁵⁶

This project contains the following underlying data:

- Data FT-IR activity in the secondary metabolite. Jarod Setiaji.pdf (Infrared spectrum of secondary metabolite extracts of heterotrophic bacteria)
- Data Inhibitory activity in the secondary metabolite. Jarod Setiaji.xlsx (Inhibitory activity in the secondary metabolite extracts of heterotrophic bacteria against pathogenic bacteria)

Data are available under the terms of the Creative Commons Attribution 4.0 International license (CC-BY 4.0).

Acknowledgments

The authors are grateful to the laboratory assistants for supporting this research.

Faculty Opinions recommended

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