Epiphytic marine pigmented bacteria: A prospective source of natural antioxidants

Pawar, Ravindra; Mohandass, Chellandi; Sivaperumal, Elakkiya; Sabu, Elaine; Rajasabapathy, Raju; Jagtap, Tanaji

doi:10.1590/S1517-838246120130353

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Brazilian Journal of Microbiology

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Environmental Microbiology • Braz. J. Microbiol. 46 (1) • Jan-Mar 2015 • https://doi.org/10.1590/S1517-838246120130353 copy

Epiphytic marine pigmented bacteria: A prospective source of natural antioxidants

Authorship SCIMAGO INSTITUTIONS RANKINGS

Awareness on antioxidants and its significance in human healthcare has increased many folds in recent time. Increased demand requisite on welcoming newer and alternative resources for natural antioxidants. Seaweed associated pigmented bacteria screened for its antioxidant potentials reveals 55.5% of the organisms were able to synthesize antioxidant compounds. DPPH assay showed 20% of the organisms to reach a antioxidant zone of 1 cm and 8.3% of the strains more than 3 cm. Pseudomonas koreensis (JX915782) a Sargassum associated yellowish brown pigmented bacteria have better activity than known commercial antioxidant butylated hydroxytoluene (BHT) against DPPH scavenging. Serratia rubidaea (JX915783), an associate of Ulva sp. and Pseudomonas argentinensis (JX915781) an epiphyte of Chaetomorpha media, were also contributed significantly towards ABTS (7.2% ± 0.03 to 15.2 ± 0.09%; 1.8% ± 0.01 to 15.7 ± 0.22%) and FRAP (1.81 ± 0.01 to 9.35 ± 0.98; 7.97 ± 0.12 to 18.70 ± 1.84 μg/mL of AsA Eq.) respectively. 16S rRNA gene sequence analysis revealed bacteria that have higher antioxidant activity belongs to a bacterial class Gammaproteobacteria. Statistical analysis of phenolic contents in relation with other parameters like DPPH, ABTS, reducing power and FRAP are well correlated (p < 0.05). Results obtained from the current study inferred that the seaweed associated pigmented bacteria have enormous potential on antioxidant compounds and need to be extracted in a larger way for clinical applications.

antioxidant; epiphytic; pigmented bacteria; seaweeds

Sr. no.	Type of algae used	Month, year and site of sample collection^* * Example: Jan-11-Vagator indicates the respective sample was collected during January-2011 from sampling site Vagator of CWCI.	Number of pigmented bacteria isolated
Chlorophyta (green algae)
1.	Caulerpa racemosa	Nov-10-Cabo De Rama	1
2.	Chaetomorpha media and Chaetomorpha antennina	Mar-10-Malvan, Mar-10-Vagator, May-10-Cabo De Rama, July-10-Malvan, July-10-Kunkeshwar, Sep-10-Malvan	8
3.	Ulva sp. and Ulva fasciata	Mar-10-Malvan, Sep-10-Vagator, July-10-Malvan, July-10-Kunkeshwar	6
Phaeophyta (brown algae)
4.	Padina boergeseniiand Padina tetrastromatica	Sep-10-Kunkeshwar, Jan-11-Malvan	3
5.	Sargassum sp., Sargassum vulgare and Sargassum ilicifolium	May-10-Cabo De Rama, Sep-10-Cabo De Rama, Sep-10-Kunkeshwar, Nov-10-Cabo De Rama, Jan-11-Vagator, May-10-Vagator	7
6.	Stechospermum marginatum	Jan-11-Kunkeshwar	1
Rhodophyta (red algae)
7.	Ceramium sp.	Mar-10-Kunkeshwar	3
8.	Gelidium micropterum	Mar-10-Malvan, May-10-Cabo De Rama, July-10-Malvan, Nov-10-Malvan	4
9.	Gracilaria corticata	Mar-10-Malvan, July-10-Kunkeshwar, Sep-10-Malvan, Sep-10-Kunkeshwar, Sep-10-Cabo De Rama, Jan-11-Vagator	3

Sr. no.	Culture code	Pigmentation	Antioxidant zone size (cm)^* * a: Colony size, b: Zone of DPPH decolorization, b-a: Final of zone of antioxidant.			Source

			a	b	b-a
1.	PIGB 1	Orange	0.4	3.1	2.7	Gelidium micropterum
2.	PIGB 10	Yellow	0.3	0.9	0.6	Gracilaria corticata
3.	PIGB 12	Yellow	0.3	0.3	0	Chaetomorpha media
4.	PIGB 13	Yellow	0.3	0.3	0	Chaetomorpha media
5.	PIGB 16	Yellow	0.2	0.2	0	Ceramium sp.
6.	PIGB 18	Red	0.6	2.5	1.9	Ceramium sp.
7.	PIGB 20	Orange	0.3	0.3	0	Ceramium sp.
8.	PIGB 28	Pale yellow	0.3	0.9	0.6	Chaetomorpha antennina
9.	PIGB 29	Pale yellow	0.2	1.1	0.9	Sargassum sp.
10.	PIGB 30	Pale yellow	0.4	0.13	0.9	Gelidium micropterum
11.	PIGB 33	Pale yellow	0.4	0.9	0.5	Sargassum ilicifolium
12.	PIGB 44	Pale yellow	1.0	2.6	1.6	Ulva fasciata
13.	PIGB 45	Yellow	0.3	0.8	0.5	Ulva fasciata
14.	PIGB 46	Pale yellow	0.5	4.0	3.5	Chaetomorpha media
15.	PIGB 47	Red/orange	0.5	2.8	2.3	Chaetomorpha media
16.	PIGB 48	Yellow	0.3	0.3	0	Chaetomorpha media
17.	PIGB 54	Pale yellow	0.2	0.2	0	Gracilaria corticata
18.	PIGB 55	Pale orange	0.3	0.3	0	Chaetomorpha media
19.	PIGB 57	Pale yellow	0.3	0.3	0	Ulva fasciata
20.	PIGB 62	Orange	0.2	0.2	0	Chaetomorpha antennina
21.	PIGB 76	Creamy	0.4	1.5	1.1	Sargassum vulgare
22.	PIGB 77	Yellowish brown	0.7	5.0	4.3	Sargassum vulgare
23.	PIGB 78	Peach	0.3	0.3	0	Gracilaria corticata
24.	PIGB 79	Orange	0.7	3.5	2.8	Padina boergesenii
25.	PIGB 80	Orange/Red	0.3	1.7	1.4	Padina boergesenii
26.	PIGB 86	Pale yellow	0.4	0.4	0	Ulva sp.
27.	PIGB 87	Creamy	0.5	1.3	0.8	Ulva sp.
28.	PIGB 88	Pink	0.5	5.4	4.9	Ulva sp.
29.	PIGB 110	Yellow	0.4	0.4	0	Gelidium micropterum
30.	PIGB 112	Creamy	0.2	0.2	0	Gelidium micropterum
31.	PIGB 115	Creamy	0.3	0.3	0	Sargassum vulgare
32.	PIGB 116	Yellow	0.2	0.2	0	Sargassum vulgare
33.	PIGB 117	Creamy	0.4	2.3	1.9	Sargassum vulgare
34.	PIGB 119	Brown	0.2	2.8	2.6	Caulerpa racemosa
35.	PIGB 126	Pale orange	0.3	0.3	0	Stechospermum marginatum
36.	PIGB 140	Pale orange	0.5	1.0	0.5	Padina tetrastromatica

Sample conc. (mg/mL)	DPPH scavenging assay (%)	EC₅₀ (mg/mL)	ABTS scavenging assay (%)	EC₅₀ (mg/mL)
Pseudomonas argentinensis (PIGB 46)
1	10.9 ± 0.28	31.13 ± 4.15	1.8 ± 0.01	46.14 ± 3.49
5	13.7 ± 0.39		4.7 ± 0.01
10	22.4 ± 0.33		8.4 ± 0.03
15	28.7 ± 0.92		15.7 ± 0.22
Pseudomonas koreensis (PIGB 77)
1	47.3 ± 0.77	1.17 ± 0.06	19.2 ± 0.05	9.41 ± 0.09
5	76.1 ± 2.61		38.9 ± 1.98
10	93.4 ± 6.54		53.4 ± 2.75
15	95.6 ± 5.61		69.5 ± 1.00
Serratia rubidaea (PIGB 46)
1	18.0 ± 0.17	10.31 ± 0.48	7.2 ± 0.03	88.34 ± 2.15
5	35.5 ± 0.32		9.3 ± 0.03
10	53.0 ± 0.56		11.3 ± 0.03
15	57.5 ± 3.03		15.2 ± 0.09
Standards
Sample conc. (μg/mL)	DPPHⁱ i DPPH scavenging assay - BHT, Scavenging assay (%)	EC₅₀ (μg/mL)	^* * Sample concentrations used for ABTS standard were 1.0, 5.0, 10.0 and 15.0 μM/mL respectively. ABTSⁱⁱ ii ABTS scavenging assay -Quercetin. scavenging assay (%)	Sample conc. (μM/mL)
40	56.6 ± 1.63	24.33 ± 1.82	78.0 ± 1.14	5.74 ± 1.26
80	80.3 ± 0.61		97.6 ± 1.25
120	82.8 ± 0.72		99.6 ± 1.18
160	84.3 ± 1.34		99.5 ± 1.06

Sample	Sample conc. (mg/mL)	FRAP assay (μg/mL of AsA Eq.)	Total phenolic content assay (mg/mL of GAE)
Pseudomonas argentinensis (PIGB 46)	1	7.97 ± 0.12	0.09 ± 0.01
	5	10.80 ± 0.13	0.17 ± 0.01
	10	14.11 ± 2.3	0.24 ± 0.02
	15	18.70 ± 1.84	0.31 ± 0.00
Pseudomonas koreensis(PIGB 77)	1	5.90 ± 0.13	0.21 ± 0.01
	5	23.26 ± 4.96	0.34 ± 0.02
	10	35.17 ± 0.36	0.65 ± 0.02
	15	47.01 ± 0.27	0.83 ± 0.05
Serratia rubidaea(PIGB 88)	1	1.81 ± 0.01	0.08 ± 0.01
	5	4.76 ± 0.05	0.21 ± 0.01
	10	7.46 ± 0.12	0.32 ± 0.01
	15	9.35 ± 0.98	0.48 ± 0.07

Isolate	Isolation source	Closest match (accession number)	Phylogenetic group	Similarity (%)	Pigmentation
PIGB 46	Chaetomorpha media	Pseudomonas argentinensis (JX915781)	γ-proteobacteria	97	Yellow
PIGB 77	Sargassum vulgare	Pseudomonas Koreensis (JX915782)	γ-proteobacteria	100	Yellow/brown
PIGB 88	Ulva sp.	Serratia rubidaea(JX915783)	γ-proteobacteria	99	Pink

Sociedade Brasileira de Microbiologia USP - ICB III - Dep. de Microbiologia, Sociedade Brasileira de Microbiologia, Av. Prof. Lineu Prestes, 2415, Cidade Universitária, 05508-900 São Paulo, SP - Brasil, Ramal USP 7979, Tel. / Fax: (55 11) 3813-9647 ou 3037-7095 - São Paulo - SP - Brazil
E-mail: bjm@sbmicrobiologia.org.br

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[1] Send correspondence to C. Mohandass. Biological Oceanography Division, CSIR-National Institute of Oceanography, Dona Paula, 403 004 Goa, Panaji, India. E-mail: cmohan@nio.org.