Recent exploration of bioactive pigments from marine bacteria

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doi: 10.2306/scienceasia1513-1874.2021.050 ScienceAsia47 (2021): 265–270

Recent exploration of bioactive pigments from marine bacteria

Tatas Hardo Panintingjati Brotosudarmo^a,∗, Leenawaty Limantara^b, Delianis Pringgenies^c

a Ma Chung Research Center for Photosynthetic Pigments (MRCPP) and Department of Chemistry, Universitas Ma Chung, Malang 65151 Indonesia

b Center for Urban Studies, Universitas Pembangunan Jaya, South Tangerang 15413 Banten, Indonesia

c Department of Marine Science, Faculty of Fisheries and Marine Science, Universitas Diponegoro, Semarang, Jawa Tengah 50275 Indonesia

∗Corresponding author, e-mail: tatas.brotosudarmo@machung.ac.id

Received 3 May 2021 Accepted 10 May 2021

ABSTRACT: Microbial pigments of marine origin are gaining increasing attention in current research due to their widely perceived applications as natural food colorants, antioxidants, antimicrobial compounds, anticancer agents, and immune stimulators. This review is a short acknowledgement of the significant progress achieved over the past five years of studies on pigments from marine bacterial isolates. Herein, we also discuss the typical challenges, as well as recent technical developments, in isolating and cultivating marine bacteria and in conducting determination of pigments as critical considerations in doing research in this field.

KEYWORDS: bioactive pigments, combinatorial approaches, culture cultivation, genome mining, marine bacteria

INTRODUCTION

Marine microorganisms, due to their rich biodiversity and genetic capacity, represent a significant source of natural product discovery[1], with success rates up to 4 times higher than other naturally derived compounds [2]. In common microbial cultures, such as marine agar, seawater-based rich media agar, and Zobell agar medium, several marine gram-positive and gram-negative bacteria appear to produce an array of pigments[3], such as carotenes (yellow to red), prodiginines (red), phenazines (yellow crystalline, deep-red solution in sulfuric acid), quinones (bright yellow), and violacein (purple).

These marine bacterial pigments are being explored for their production, which is clinically and indus- trially important because they have demonstrated various biological activities, such as antioxidant, antimicrobial, and anticancer, as well as acting to stimulate immunity[4].

In the 1960s, research on natural marine products began to flourish[5], primarily due to advances in instrumentation for structure elucidation, particularly the mass spectrometry, and isolation techniques as well as the availability of scuba gear for the collection of marine organisms at certain depths.

Highlights of achievements have been frequently reviewed and indicate the structural complexity and

Fig. 1 Search results using the keyword “novel pigment;

marine bacteria” in the search engine provided by https://

pubmed.ncbi.nlm.nih.gov/ from 1975 to 2021 for journal articles.

potent biological activities of these pigments. In the PubMed search engine, using the keyword “novel pigments; marine bacteria”, the number of articles reporting on bacterial marine pigments increased from only 8 articles in 2002 to 84 articles by 2015 (Fig. 1). These articles include research on the isolation and determination of new compounds and on new bacterial species or strains, research on bioactivity assays and therapeutic studies of pigments, and review articles. The number of pub-

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266 ScienceAsia47 (2021)

lished articles on marine bacterial pigments has shown a rather downhill trend since 2015, despite the untapped potential of marine biodiversity.

HIGHLIGHTS DURING THE PAST FIVE YEARS The most recent pigments that were extracted from marine bacterial isolates that have been characterized in the past five years are listed in Table 1.

At least 17 species have been successfully isolated from their native habitat, including in seawater, sediments, and in association or affiliation with marine invertebrates. It has been extensively reviewed that marine sediment holds untapped potential for novel taxonomic and bioactive bacterial diversity comparable to seawater[6], in which both aerobic and anaerobic microbial ecosystems exist that per- sist on very low fluxes of bioavailable energy over geologic time[7]. It was reported that seawater and sediments comprise a similar number of distinct bacterial species with a mean± standard deviation (SD) of 1378± 61 species for seawater and 1452 ± 74 species for sediments [6]. Living together and using invertebrates as hosts and microorganisms as symbionts is also common in marine environ- ments[8]. Marine invertebrates, particularly sessile invertebrates, often rely upon chemical defence, and symbiosis with biochemically versatile microorganisms is an efficient strategy for survival[9]. In the absence of their microbial symbionts, most marine invertebrates cannot survive [10,11]. Microbial symbionts have been shown to produce a variety of tailored biochemical traits due to coevolution with their specific host, making them a rich source of secondary metabolites, particularly pigments with medically and commercially attractive bioactivities [12–14].

Several new and rare compounds have been characterized over the past five years (Table 1).

Carotenoids are a family of yellow to orange-red pigments, generally comprising a 40-carbon skeleton composed of 8-isoprene units. In carotenoid groups, seven rare compounds include the C₄₅ and C₅₀ carotenoids. By 2017, more than 250 carotenoids of marine origin had been identified[15], and the unique compositions present in marine microorganisms have promoted the use of carotenoids as a chemical signature for rapid chemotaxonomic profiling. Six new and rare carotenoids that have been reported in the past five years include 2⁰- isopentenyldehydrosaproxanthin (C₄₅ carotenoid) from Arthrobacter sp. P40 [16], decaprenoxanthin and its glucosylated derivatives (C₅₀ carotenoids)

from Rhodopirellula rubra LF2^T [17], and zeax- anthin sulfate from Erythrobacter flavus KJ5 [18].

Newly identified marine bacteria that produce high levels of astaxanthin and its derivatives, such as 2⁰-hydroxyastaxanthin and 2,2⁰-dihydroxy- astaxanthin, have also been reported[19,20]. The unique structure of astaxanthin, which contains both a keto group and hydroxyls, plays an important role in neutralizing reactive oxygen species (ROS) [21].

Newly characterized bioactive pigments from the quinone group have also been reported, such as fridamycins H and fridamycins I from Acti- nokineospora spheciospongiae sp. nov., along with three known compounds, actinosporins C, D, and G [22]. Mersaquinone, a new tetracene derivative that exhibits antibacterial activity against methicillin-resistant Staphylococcus aureus, was suc- cessfully characterized and reported [23]. In addition, two new polycyclic anthraquinones, N- acetyl-N demethyl-mayamycin and Streptoanthra- quinone A, were found in Streptomyces sp. 182SMLY, which were successfully isolated from a sample of marine sediment at a 3.6 m depth [24]. Al- though prodiginines were initially identified from the terrestrial bacterium Serrantia marcescens, these compounds were subsequently obtained from several bacteria in different marine habitats, such as Pseudomonas rubra strains PS1 and SB14, which were isolated from seawater [25], and Zooshikella sp. and Streptomyces sp. that were isolated from sediment [26]. Phenazine pigments, including phenazine-1-carboxylic acid and pyocyanin, were successfully characterized from Pseudomonas aerug- inosa isolated from sediment [27,28]. New Pseu- doalteromonas byunsanensisstrains JW1T and JW3 isolated from surface seawater were found to produce violacein[29].

MAIN CHALLENGES

The low percentage of microbes that can be readily cultured and sustainably grown under laboratory conditions is one of the primary hurdles to contin- ued characterization of bioactive pigments. In fact, more than 99% of marine microorganisms have not been successfully cultured under laboratory conditions [30]. Approximately 107 types of bacteria were isolated from one gram of sediment, and only 5% of those microorganisms were able to be grown in the lab [31]. This phenomenon is referred to as the “great plate count anomaly” [32], a term to describe differences in the order of magnitude

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Table 1 Most recent bio-pigments extracted from marine bacterial isolates have been characterized in the last five years.

Pigment Chemical λmax Molecular Marine bacterial Therapeutic Ref.

Formula (nm) ion (m/z) species application

Carotenoid group

Decaprenoxanthin C₅₀H₇₂O₂ 417, 442, 471 705.6[M+H]⁺ Arthrobactersp. P40 Antioxidant [17] Decaprenoxanthin

monoglucoside

C₅₆H₈₂O₇ 417, 442, 471 867.6[M+H]⁺ Arthrobactersp. P40 Antioxidant [17] Decaprenoxanthin

diglucoside C₆₂H₉₂O₁₂ 417, 442, 471 1029.6[M+H]⁺ Arthrobactersp. P40 Antioxidant [17]

2⁰-Hydroxy- astaxanthin

C₄₀H₅₂O₅ 478 613[M+H]⁺ Brevundimonassp. strain N-5 Antioxidant [19] 2,2⁰-Dihydroxy-

astaxanthin

C₄₀H₅₂O₆ 478 629.0[M+H]⁺ Brevundimonas scallop Brevundimonassp. strain N-5

Antioxidant [19,20] Dehydroflexixanthin C₄₀H₅₂O₃ – 581[M+H]⁺ Rhodopirellula rubraLF2^T Antioxidant [16] 2⁰-Isopentenyldehy-

drosaproxanthin

C₄₅H₆₄O₂ 470, 500 637[M+H]⁺ Rhodopirellula rubraLF2^T Antioxidant [16] Saproxanthin C₄₀H₅₆O₂ 444, 470, 500 590[M+Na]⁺ Rhodopirellula rubraLF2^T

Rubinisphaera brasiliensisGr7

Antioxidant [16] Zeaxanthin-sulfate C₄₀H₅₅SO₅Na 427, 453, 481 648.5[M−Na]⁻ Erythrobacter flavusKJ5 Antioxidant [18,41] Quinone group

Bisantraquinone 1 C₃₂H₂₅O₉ 229, 261, 287, 361, 415

553.15[M+H]⁺ Ecteinascidia turbinada Antibacterial

Anticancer [44] Fridamycins H C₂₅H₂₆O₁₁ 231, 253, 293 503.15[M+H]⁺ Actinokineospora spheciospon-

giaesp. nov. Antitrypanosomal [22]

Fridamycins I C₃₂H₃₃NO₁₀Na 232, 253, 294 614[M+H]⁺ Actinokineospora spheciospon- giaesp. nov.

Antitrypanosomal N-acetyl-N demethyl-

mayamycin

C₂₇H₂₅NO₈ 328, 443 514.15[M+Na]⁺ Streptomycessp. 182SMLY Antibacteria [24] Mersaquinone C₁₉H₁₂O₆ 218, 277, 308,

350, 480, 515, 550

337.07[M+H]⁺ Streptomycessp. Antibacterial [23]

Streptoanthra- quinone A

C₂₈H₂₂O₈ 220, 330, 445 509.12[M+Na]⁺ Streptomycessp. 182SMLY Antibacterial [24]

Prodigiosin group

Prodigiosin C₂₀H₂₅N₃O 537 324.4[M+H]⁺ Pseudomonas rubrastrain PS1 and SB14

Zooshikellasp.

Streptomycessp.

Antibacterial Anticancer Anti- inflammatory

[25,26]

Phenazine group Phenazine-1- carboxylic acid

C₁₃H₈N₂O₂ 252, 365, 354 247.05[M+Na]⁺ Pseudomonas aeruginosa strain PA31x

Antibacterial

Antifungal [27] Pyocyanin C₁₃H₁₁N₂O 201, 238, 318,

710, 886

211[M]⁺ Pseudomonas aeruginosa Antibacterial [28,45]

Violacein group

Violacein C₂₀H₁₃N₃O₃ 585 344.12[M+H]⁺ Janthinobacterium lividum Chromobacterium violaceum Pseudoalteromonas byunsanensis

Antimicrobial

Anticancer [29,46,47]

between the numbers of cells from the natural envi- ronment that form colonies on agar media and the number countable by microscopic examination. Un- fortunately, in marine ecosystems, only 0.01 to 0.1%

of oceanic marine bacterial cells produce colonies using standard plating techniques [33]. The next challenge is achieving an adequate amount of the desired metabolites to allow identification of bacterial bioactive pigments and their bioactivity, a tedious process [34]. Another challenge in this research corresponds to genome mining. As the number of available genomes is increasing, genome mining is becoming a challenging method to identify new natural products and to validate data[35].

DEVELOPMENTS AND CONSIDERATIONS

There are a number of reasons that marine microorganisms are difficult to cultivate in the laboratory, including a lack of adequate growth conditions, low growth rates, poor development of colonies, requirement for metabolites generated by other microbes, and the presence of dormant cells[36]. Var- ious cultivation strategies have been proposed and reviewed, such as the in situ cultivation technique that uses diffusion chambers, microbial traps, iChip (isolation chip), iTip (in situ cultivation by tip), and double encapsulation techniques[37]. Another promising new cultivation and screening strategy

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with the advantages of being high throughput, mi- croscale, single-cell resolution, and automation potential, called the microfluidic droplet-based technique, has also been introduced[38].

Inducing stress or external stimulation has been a recent research trend and strategy to increase pigment production in the biotechnological process;

for example, enhanced production of pyocyanin from Pseudomonas aeruginosa was successful with cottonseed meal [39]. The blue, yellow, white, green, incandescent lamp, red halogen, and fluores- cence lamp were used for enhancing the carotenoid content, or another example using gamma radiation for an enhanced production of prodigiosin[40].

Recently, combinatorial approaches using si- multaneous bioinformatics, genetics, and analytical tools have introduced new strategies for the discovery of bioactive pigments from marine bacterial isolates. As all pigments have a genetic basis, the ability to obtain and interpret genetic information have been the first step in daily based protocol for structural elucidation, a process that is increasingly available at low cost to non-specialists.

Setiyono et al [18] applied analysis of the complete genome sequence of the marine bacterium Erythrobacter flavus strain KJ5 [41] to reveal the possibility of a new carotenoid present, by com- paring the carotenoids composition produced by E. longus and E. nanhaesediminis, members of the genus Erythrobacter that have close sequence simi- larity and were therefore assumed to have a similar carotenoid biosynthesis pathway. Identification of sulfate attachment to the zeaxanthin carotenoid was then resolved by a tandem mass spectrometry (MS/MS) detected in negative ion mode using multiple reaction monitoring (MRM). Another example showed that BLAST analysis of antimicro- bial prodiginine pigments from Pseudomonas rubra strains PS1 and SB14 to identify highly similar sequences (megablast) resulted in identification of two primary pigments, prodigiosin and cycloprodi- giosin, and their derivatives [25]. Recently, with genome mining, the process of extracting information from genome sequences to detect biosynthetic pathways of bioactive natural products and their possible functional and chemical interactions has become available[35].

In combination with liquid chromatography (LC), mass spectrometry has become the gold standard for a high-throughput qualitative and quantitative profiling of natural product compounds [42], especially pigments. Other hyphen- ated technique such as nuclear magnetic reso-

nance coupled with LC (LC-NMR) is also useful analytical platforms for detection, identification, and quantification of compounds in extracts.

NMR analysis is reproducible and provides de- tailed structural information, although it generally profiles only major constituents, in other words, it has relatively low sensitivity. Thou- sands of sets of MS/MS data have been recorded and continuously developed in publicly accessible databases. Open-access knowledge bases containing tandem mass spectrometry, such as the Global Natural Products Social Molecular Networking (GNPS, https://gnps.ucsd.edu/ProteoSAFe/static/

gnps-splash.jsp) and the Natural Product Atlas (https://www.npatlas.org/joomla/), which provide a tool to explore the structure of microbial natural products, are available and have greatly enhanced the efficiency of the replication processes, leading to identification of new molecules[43]. Specifically, for the carotenoid group, the Carotenoid Database (http://carotenoiddb.jp/), at the time of writing, provides information on 1204 natural carotenoids in 722 source organisms, including their biosynthetic pathways, structures and similarity search, and some biological activities.

Acknowledgements: This work was supported by fund- ing from the Directorate of Research and Community Services, Ministry of Research and Technology/National Research and Innovation Agency of the Republic of In- donesia under World Class Research scheme grant number 001/MACHUNG/LPPM/SP2H-LIT-MONO/IV/2021.

REFERENCES

1. Joye S, Kostka JE (2020) Microbial Genomics of the Global Ocean System. American Academy of Microbi- ology, Washington DC.

2. Sigwart JD, Blasiak R, Jaspars M, Jouffray J-B, Tas- demir D (2021) Unlocking the potential of marine biodiscovery. Nat Prod Rep.

3. Ramesh C, Vinithkumar NV, Kirubagaran R (2019) Marine pigmented bacteria: A prospective source of antibacterial compounds. J Nat Sci Biol Med 10, 104–113.

4. Velmurugan P, Veni CK, Ravi AV (2020) Marine bacteria is the cell factory to produce bioactive pigments:

A prospective pigment source in the ocean. Front Sustain Food Syst4, ID 589655.

5. Dias DA, Jones OAH, Beale D, Boughton BA, Benheim D, Kouremenos KA, Wolfender J, Wishart DS (2016) Current and future perspectives on the structural identification of small molecules in biological sys- tems. Metabolites 6, ID 46.

6. Bech PK, Lysdal KL, Gram L, Bentzon-Tilia M, Strube ML (2020) Marine sediments hold an untapped po-

www.scienceasia.org

(7)

ScienceAsia47 (2021) 269

tential for novel taxonomic and bioactive bacterial diversity. mSystems 5, e00782-20.

7. Hoshino T, Doi H, Uramoto GI, Wörmer L, Adhikari RR, Xiao N, Morono Y, D’Hondt S, etal (2020) Global diversity of microbial communities in marine sedi- ment. Proc Natl Acad Sci USA 117, 27587–27597.

8. Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: The art of harnessing chemosynthesis. Nat Rev Microbiol 6, 725–740.

9. Flórez LV, Biedermann PHW, Engl T, Kaltenpoth M (2015) Defensive symbioses of animals with prokary- otic and eukaryotic microorganisms. Nat Prod Rep 32, 879–1156.

10. Stanley JT, Castenholz RW, Colwell RR, Holt JG, Kane MD, Pace NR, Salyers AA, Tiedje JM (1997) The Microbial World: Foundation of the Biosphere.

American Academy of Microbiology, Washington DC.

11. Brien PAO, Webster NS, Miller DJ, Bourne DG (2019) Host-microbe coevolution: applying evidence from model systems to complex marine invertebrate holo- bionts. MBio 10, e02241-18.

12. Blockley A, Elliott DR (2017) Symbiotic microbes from marine invertebrates: Driving a new era of natural product drug discovery. Diversity 9, ID 49.

13. Zhang X, Wei W, Tan R (2015) Symbionts, a promis- ing source of bioactive natural products. Sci China Chem58, 1097–1109.

14. Torregrosa-crespo J, Montero Z, Fuentes JL, Reig M, Carlos V, Martinez-Espinosa RM (2018) Exploring the valuable carotenoids for the large-scale production by marine microorganisms. Mar Drugs 16, ID 203.

15. Galasso C, Corinaldesi C, Sansone C (2017) Carotenoids from marine organisms: Biological functions and industrial applications. Antioxidants 6, ID 96.

16. Kallscheuer N, Moreira C, Airs R, Llewellyn CA, Wie- gand S, Jogler C, Lage OM (2019) Pink- and orange- pigmented Planctomycetes produce saproxanthin- type carotenoids including a rare C45 carotenoid.

Environ Microbiol Rep11, 741–748.

17. Vila E, Hornero-Méndez D, Azziz G, Lareo C, Saravia V (2019) Carotenoids from heterotrophic bacteria isolated from Fildes Peninsula, King George Island, Antarctica. Biotechnol Rep 21, e00306.

18. Setiyono E, Heriyanto, Pringgenies D, Shioi Y, Kane- saki Y, Awai K, Brotosudarmo THP (2019) Sulfur- containing carotenoids from a marine coral symbiont Erythrobacter flavusstrain KJ5. Mar Drugs 17, ID 349.

19. Asker D (2017) Isolation and characterization of a novel, highly selective astaxanthin-producing marine bacterium. J Agric Food Chem 65, 9101–9109.

20. Liu H, Zhang C, Zhang X, Tan K, Zhang H, Cheng D, Ye T, Li S, et al (2020) A novel carotenoids-producing marine bacterium from noble scallop Chlamys nobilis and antioxidant activities of its carotenoid composi- tions. Food Chem 320, ID 126629.

21. Brotosudarmo THP, Limantara L, Setiyono E,

Heriyanto (2020) Structures of astaxanthin and their consequences for therapeutic application. Int J Food Sci2020, 14–17.

22. Tawfike A, Attia EZ, Desoukey SY, Hajjar D, Makki AA, Schupp PJ, Edrada-Ebel RA, Abdelmohsen UR (2019) New bioactive metabolites from the elicited marine sponge-derived bacterium Actinokineospora spheciospongiaesp. nov. AMB Express 9, ID 12.

23. Kim MC, Cullum R, Hebishy AMS, Mohamed HA, Faraag AHI, Salah NM, Abdelfattah MS, Fenical W (2020) Mersaquinone, a new tetracene derivative from the marine-derived Streptomyces sp. EG1 ex- hibiting activity against methicillin-resistant Staphy- lococcus aureus(MRSA). Antibiotics 9, ID 252.

24. Liang Y, Xie X, Chen L, Yan S, Ye X, Anjum K, Huang H, Lian X, et al (2016) Bioactive polycyclic quinones from marine Streptomyces sp. 182SMLY. Mar Drugs 14, ID 10.

25. Setiyono E, Adhiwibawa MAS, Indrawati R, Pri- hastyanti MUU, Shioi Y, Brotosudarmo THP (2020) An Indonesian marine bacterium, Pseudoalteromonas rubra, produces antimicrobial prodiginine pigments.

ACS Omega5, 4626–4635.

26. Ramesh C, Vinithkumar NV, Kirubagaran R, Ve- nil CK, Dufoseé L (2020) Applications of prodigiosin extracted from marine red pigmented bacteria Zooshikella sp. and Actinomycete Streptomyces sp.

Microorganisms8, ID 556.

27. Zhang L, Tian X, Kuang S, Liu G, Zhang C, Sun C (2017) Antagonistic activity and mode of action of phenazine-1-carboxylic acid, produced by marine bacterium Pseudomonas aeruginosa PA31x, against Vibrio anguillarum in vitroand in a zebrafish in vivo model. Front Microbiol 8, ID 289.

28. DeBritto S, Gajbar TD, Satapute P, Sundaram L, Lak- shmikantha RY, Jogaiah S, Ito S (2020) Isolation and characterization of nutrient dependent pyocyanin from Pseudomonas aeruginosa and its dye and agro- chemical properties. Sci Rep 10, ID 1542.

29. Wu YH, Cheng H, Xu L, Jin XB, Wang CS, Xu XW (2017) Physiological and genomic features of a novel violacein-producing bacterium isolated from surface seawater. PLoS One 12, e0179997.

30. Jiao JY, Liu L, Hua ZS, Fang BZ, Zhou EM, Salam N, Hedlund BP, Li WJ (2021) Microbial dark matter coming to light: Challenges and opportunities. Natl Sci Rev8, ID nwaa280.

31. Sun W, Wu W, Liu X, Zaleta-Pinet DA, Clark BR (2019) Bioactive compounds isolated from marine- derived microbes in China: 2009–2018. Mar Drugs 17, ID 339.

32. Staley JT, Konopka A (1985) Microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 39, 321–346.

33. Connon SA, Giovannoni SJ (2002) High-throughput methods for culturing microorganisms in very-low- nutrient media yield diverse new marine isolates.

www.scienceasia.org

(8)

Appl Environ Microbiol68, 3878–3885.

34. Joint I, Mühling M, Querellou J (2010) Culturing marine bacteria: An essential prerequisite for biodis- covery: Minireview. Microb Biotechnol 3, 564–575.

35. Albarano L, Esposito R, Ruocco N, Costantini M (2020) Genome mining as new challenge in natural products discovery. Mar Drugs 18, ID 199.

36. Overmann J, Lepleux C (2016) Marine bacteria and archaea: Diversity, adaptations, and culturability. In:

Stal LJ, Cretoiu MS (eds) The Marine Microbiome: An Untapped Source of Biodiversity and Biotechnological Potential, Springer International Publishing, Switzer- land, pp 21–56.

37. Wang F, Li M, Huang L, Zhang XH (2021) Cultivation of uncultured marine microorganisms. Mar Life Sci Technol3, 117–120.

38. Hu B, Xu B, Yun J, Wang J, Xie B, Li C, Yu Y, Lan Y, et al (2020) High-throughput single-cell cultivation reveals the underexplored rare biosphere in deep- sea sediments along the Southwest Indian Ridge. Lab Chip20, 363–372.

39. El-Fouly MZ, Sharaf AM, Shahin AAM, El-Bialy HA, Omara AMA (2015) Biosynthesis of pyocyanin pig- ment by Pseudomonas aeruginosa. J Radiat Res Appl Sci8, 36–48.

40. Chatragadda R, Dufossé L (2021) Ecological and biotechnological aspects of pigmented microbes: A way forward in development of food and pharma- ceutical grade pigments. Microorganisms 9, ID 637.

41. Kanesaki Y, Setiyono E, Pringgenies D, Moriuchi

R, Brotosudarmo THP, Awai K (2019) Complete genome sequence of the marine bacterium Ery- throbacter flavus strain KJ5. Microbiol Resour An- nounc8, e00140-19.

42. Atanasov AG, Zotchev SB, Dirsch VM, Orhan IE, Banach M, Rollinger JM, Barreca D, Weckwerth W, et al (2021) Natural products in drug discovery:

Advances and opportunities. Nat Rev Drug Discov 20, 200–216.

43. Rotter A, Barbier M, Bertoni F, Bones AM, Cancela ML, Carlsson J, Carvalho MF, Cegłowska M, et al (2021) The essentials of marine biotechnology. Front Mar Sci8, ID 629629.

44. Ghareeb MA, Tammam MA, El-Demerdash A, Atanasov AG (2020) Insights about clinically approved and preclinically investigated marine natural products. Curr Res Biotechnol 2, 88–102.

45. Li JL, Yang N, Huang L, Chen D, Zhao Y, Tang MM, Fan H, Bao X (2018) Pyocyanin inhibits Chlamydia infection by disabling infectivity of the elementary body and disrupting intracellular growth. Antimicrob Agents Chemother62, e02260-17.

46. Arif S, Batool A, Khalid N, Ahmed I, Janjua HA (2017) Comparative analysis of stability and biological activities of violacein and starch capped silver nanoparticles. RCS Adv 7, 4468–4478.

47. Choi SY, Lim S, Yoon K, Lee JI, Mitchell RJ (2021) Biotechnological activities and applications of bacte- rial pigments violacein and prodigiosin. J Biol Eng 15, ID 10.

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February 15, 2020

Professor Dr. Tatas Brotosudarmo Department of Chemistry

Machung University Indonesia

Dear Professor Brotosudarmo

ScienceAsia has recently initiated to publish the review articles written by renowned scientists in various science fields within the journal scope. As our Board member with expertise in Chemistry of photosynthetic pigments, an area of wide interest, it is our honor to invite you to contribute a mini review article of your expertise. We do hope you will accept our invitation for the benefits of our wide readership.

The length of the manuscript should be around 10-12 pages A4, 1.5 space, including Figures, Tables and Reference section. Please follow the Instructions for Authors and/or the previous review articles in issues 46/47 of 2020/2021. We anticipate having your manuscript published in volume 47 (4) (August issue of 2021), please kindly send your manuscript to editor@scienceasia.org by July 1, 2021.

Please receive our appreciation for your kind contribution to ScienceAsia.

Best regards

Piamsook Pongsawasdi, Emeritus Prof.

Editor-in-Chief, ScienceAsia

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21.5.2021 Email - Tatas H.P Brotosudarmo, Ph.d - Outlook

https://outlook.office.com/mail/id/AAQkADRmN2NkMzA3LTgxNDMtNGU5Yi05ZjM2LTNhNjNlOWRjYmQ1NQAQADK5eaSdLR1Gs4aXO7LYXss%… 1/5

RE: Invitation to write review article for ScienceAsia Piamsook Pongsawasdi <Piamsook.P@chula.ac.th>

Tue 20/04/2021 10:25 AM

To: Tatas H.P Brotosudarmo, Ph.d <tatas.brotosudarmo@machung.ac.id>

Thank you very much for your positive response. I will wait for your MS.

Piamsook Pongsawasdi

Emeritus Prof, Department of Biochemistry Faculty of Science

Chulalongkorn University Bangkok 10330

THAILAND

________________________________________

From: Tatas H.P Brotosudarmo, Ph.d [tatas.brotosudarmo@machung.ac.id]

Sent: Monday, April 19, 2021 6:02 PM To: Piamsook Pongsawasdi

Subject: Re: Invitation to write review article for ScienceAsia Dear Prof. Pongsawasdi,

Yes, this short review will stress on scientific aspects of the exploration, acknowledging the significant progress achieved, discuss the typical challenges and recent development in isolating and cultivating marine bacteria, and conducting the determination of pigments as critical considerations.

I think I will be finished by May 15. I will send the manuscript by e-mail to editor@scienceasia.org.

Sincerely yours, Tatas

---

Tatas Hardo Panintingjati Brotosudarmo, Dipl.Chem., Ph.D.

Principal Investigator

Pigments & Metabolism Research Group

Ma Chung Research Center for Photosynthetic Pigments (MRCPP) Designated as an Indonesia Higher Education – Center of Excellence

(Directorate of Higher Education Institutional Enhancement, RISTEKDIKTI No.

T/3768/C5/KB.07.00/2019) Associate Professor

Department of Chemistry Universitas Ma Chung Villa Puncak Tidar N-01 Malang 65151 Jawa Timur Indonesia

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T:+62 341 550 171 ext. 4310 F:+62 341 550 175

URL: http://mrcpp-people.machung.ac.id/brotosudarmo-thp/home

<http://www.inadc-phei.org>

________________________________

From: Piamsook Pongsawasdi <Piamsook.P@chula.ac.th>

Sent: 17 April 2021 2:28 PM

To: Tatas H.P Brotosudarmo, Ph.d <tatas.brotosudarmo@machung.ac.id>

Subject: RE: Invitation to write review article for ScienceAsia Dear Dr Brotosudarmo

From the proposed title, I hope the content will stress on scientific aspects of the exploration, especially on chemistry of bioactive pigments and marine organism involved.

You can submit through the journal website, or by sending as email attached file to the journal email (editor@scienceasia.org).

By the way, would you be able to finish before the due date I asked you (June 1 for August issue)? In case you can submit by May 15, your article will be published in June issue instead of August issue.

Please give me a reply whether you can submit earlier or not.

Regards Piamsook

Piamsook Pongsawasdi Editor-in-Chief, ScienceAsia

THAILAND

________________________________________

Sent: Friday, April 16, 2021 9:10 PM To: Piamsook Pongsawasdi

Subject: Re: Invitation to write review article for ScienceAsia Dear Prof Pongsawasdi,

Herewith I would like to inform you of the tentative title of my mini-review article: "Critical

consideration of the exploration of bioactive pigments from marine bacteria over the past five years".

Could you please inform me how to submit the manuscript? May I submit it directly via the website?

Sincerely yours, Tatas

---

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T:+62 341 550 171 ext. 4310 F:+62 341 550 175

________________________________

Sent: 17 February 2021 10:58 AM

Subject: RE: Invitation to write review article for ScienceAsia Dear Prof Brotosudarmo

Thank you very much for your kind acceptation to write a review article for us. Please give me the tentative title of your article at least a month before the due date of submission.

May I give you a bit more information on the detail format of the manuscript. For the invited minireview article, total number of page (including Figures, Tables, and References) is around 10-12 A4 pages (line space 1.5), however, it could be longer up to 20 pages. Abstract should not exceed 250 words. Maximum number of references should not exceed 70 (or up to 80), style of writing

References in the Reference list follows the Instructions for Authors on our website

([http://www.scienceasia.org<http://www.scienceasia.org<http://www.scienceasia.org<http://www.sci enceasia.org]www.scienceasia.org<http://www.scienceasia.org<http://www.scienceasia.org<http://w ww.scienceasia.org>>). In the invited review articles, we expect the author(s) to mention about their works related to the topic with at least having their publications cited in about 10-20% of the total number of References. And it is good to cite some ScienceAsia articles related (especially those published in 2019-2021), if any. Overall format could be found in previous review articles already published in 2019-2021.

Kind Regards Piamsook

(13)

THAILAND

________________________________________

Sent: Tuesday, February 16, 2021 7:59 PM To: Piamsook Pongsawasdi

Subject: Re: Invitation to write review article for ScienceAsia Dear Professor Piamsook Pongsawasdi,

I am very indebted to be invited to write a review article for ScienceAsia.

I will prepare an article for it.

With kind regards, ---

T:+62 341 550 171 ext. 4310 F:+62 341 550 175

(14)

________________________________

Sent: 16 February 2021 10:44 AM

Subject: Invitation to write review article for ScienceAsia Dear Prof Brotosudarmo

Please receive our invitation letter in the attached file.

Hope to have your response soon.

Best Regards Piamsook

THAILAND

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21.5.2021 ScienceAsia - Journal of The Science Society of Thailand

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ACCEPTED ARTICLES Table of Contents Accepted articles are publish online and citable using thei numbers. Volumes and issu be published will be further assigned.

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21.5.2021 ScienceAsia

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ScienceAsia

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SCOPE

ScienceAsia is a multidisciplinary journal publishing papers of high quality bimonthly, in printed and electronic versions, by the Scie of Thailand under Royal Patronage and the National Research Council of Thailand. The journal publishes original research papers t novel ndings and important contribution to broad area in science and mathematics. Areas covered include Biological Sciences an Biotechnology, Chemistry and Material Sciences, Environmental and Applied Sciences, and Mathematics and Physical Sciences. M may report scienti cally useful data, observations or model predictions, and/or provide a new scienti c concept or a new explanat published results. Submissions of materials of current scienti c interest are highly welcome, provided that there is su cient scien The journal will not accept manuscripts which have been published or are being considered for publication elsewhere, nor should m being considered by ScienceAsia be submitted to other journals. Submitted manuscripts must conform to the guidelines given in t Instructions for Authors

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Cites per document Year Value Cites / Doc. (4 years) 2006 0.000 Cites / Doc. (4 years) 2007 0.167 Cites / Doc. (4 years) 2008 0.537 Cites / Doc. (4 years) 2009 0.548 Cites / Doc. (4 years) 2010 0.907 Cites / Doc. (4 years) 2011 1.419 Cites / Doc. (4 years) 2012 1.547 Cites / Doc. (4 years) 2013 1.708 Cites / Doc. (4 years) 2014 1.467 Cites / Doc. (4 years) 2015 1.405 Total Cites Self-Cites

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Evolution of the number of total citation per document and external citation per document (i.e. journal self- citations removed) received by a journal's published documents during the three previous years. External citations are calculated by subtracting the number of self-citations from the total number of citations received by the journal’s documents.

% International Collaboration

International Collaboration accounts for the articles that have been produced by researchers from several countries. The chart shows the ratio of a journal's documents signed by researchers from more than one country; that is including more than one country address.

Year International Collaboration 2006 21 67

Citable documents Non-citable documents

Not every article in a journal is considered primary research and therefore "citable", this chart shows the ratio of a journal's articles including substantial research (research articles, conference papers and

Cited documents Uncited documents

Ratio of a journal's items, grouped in three years windows, that have been cited at least once vs. those not cited during the following year.

2007 2009 2011 2013 2015 2017 2019 0.07

0.14 0.21 0.28

Cites / Doc. (4 years) Cites / Doc. (3 years) Cites / Doc. (2 years)

2006 2008 2010 2012 2014 2016 2018 2020 0

0.4 0.8 1.2 1.6 2

2006 2008 2010 2012 2014 2016 2018 2020 0

200 400

2006 2008 2010 2012 2014 2016 2018 2020 0

0.9 1.8

2006 2008 2010 2012 2014 2016 2018 2020 0

20 40

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Metrics based on Scopus® data as of April 2021

Zubair Ali Shah 2 years ago Dear Editor,

I hope you are doing well.

We submitted the paper entitled with "Theoretical framework of the Modi ed Organic Rankine Cycles for improved energy and exergy performances" on 26 may 2019 but still not received any response after the acknowledgement of submission.

Hope to hear from you soon.

manuscript MS No. 2019-0434 Regards,

Zubair Ali Shah reply

Toansakul Tony Santiboon 3 years ago

Department of Biotechnology, Faculty of Technology, Mahasarakham University, Mahasarakham 44150

14 September 2018

Dear Editor Broad of Food Chemistry

We are the author team of our research manuscript, it’s title as “Synbiotic Ice Cream Containing reviews) in three year windows vs. those documents

other than research articles, reviews and conference papers.

Documents Year Value

Uncited documents 2006 0 Uncited documents 2007 56 Uncited documents 2008 99

U it d d t 2009 150

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https://outlook.office.com/mail/id/AAQkADRmN2NkMzA3LTgxNDMtNGU5Yi05ZjM2LTNhNjNlOWRjYmQ1NQAQAIMVJJub%2FrdNqDCYLM0DlR… 1/1

Submit Mini Review Science Asia

Tatas H.P Brotosudarmo, Ph.d <tatas.brotosudarmo@machung.ac.id>

Mon 03/05/2021 8:01 PM

To: editor@scienceasia.org <editor@scienceasia.org>

1 attachments (341 KB)

ScienceAsia_manuscript_030521.doc;

Dear Prof Piamsook Pongsawasdi,

I am very indebted to be invited to write a review about my research ﬁeld. With this e-mail, I would like to submit the manuscript en tled "Cri cal considera on of the explora on of bioac ve pigments from marine bacteria over the past ﬁve years".

On behalf of the authors, we do hope that this manuscript will meet your criteria and we believe that these insights will be of keen interest to the broad readership of Science Asia, par cularly those who have an interest in the natural product chemistry, i.e. bioac ve pigments, from marine

resources.

Sincerely yours,

---

Ma Chung Research Center for Photosynthetic Pigments (MRCPP) Designated as an Indonesia Higher Educa on – Center of Excellence

(Directorate of Higher Educa on Ins tu onal Enhancement, RISTEKDIKTI No. T/3768/C5/KB.07.00/2019) Associate Professor

T:+62 341 550 171 ext. 4310 F:+62 341 550 175