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Proceeding Paper

Evidence and Perspectives on the Use of Phlorotannins as Novel Antibiotics and Therapeutic Natural Molecules †

1
Nutrition and Bromatology Group, Department of Analytical and Food Chemistry, Faculty of Food Science and Technology, Ourense Campus, University of Vigo, E32004 Ourense, Spain
2
Centro de Investigação de Montanha (CIMO), Instituto Politécnico de Bragança, Campus de Santa Apolonia, 5300-253 Bragança, Portugal
3
Department for Sustainable Food Process, Università Cattolica del Sacro Cuore, Via Emilia Parmense 84, 29122 Piacenza, Italy
4
LAQV-REQUIMTE Department of Chemistry and Biochemistry, Faculty of Sciences, University of Porto, Rua do Campo Alegre s/n, 4169-007 Porto, Portugal
5
Centro de Investigación e Innovación Tecnológico en Algas Marinas (CIITAM), Algas Atlánticas Algamar S.L., Polígono de Amoedo, Pazos de Borbén, E36840 Pontevedra, Spain
*
Authors to whom correspondence should be addressed.
Presented at the 2nd International Electronic Conference on Antibiotics—Drugs for Superbugs: Antibiotic Discovery, Modes of Action and Mechanisms of Resistance, 15–30 June 2022; Available online: https://eca2022.sciforum.net/.
Med. Sci. Forum 2022, 12(1), 43; https://doi.org/10.3390/eca2022-12728
Published: 15 June 2022

Abstract

:
Multiple drug-resistant bacterial strains are showing new different mechanisms to overcome the antimicrobial action, which reduces the efficacy of conventional antibiotics. Therefore, drug discovery research has focused on developing fast, effective, and safe alternatives to prevent this multi-resistance. Phlorotannins are a diverse class of polyphenols, secondary metabolites described in brown algae, that are mainly constituted of polymers of phloroglucinol and, depending on their linkage and structure, can be classified mainly as fucols, fucophlorethols, eckols, and phloroethols. These polyphenols have been described in both macro- and microalgae, suggesting that they can be recovered from a great variety of sources. Phlorotannins have been extensively described to possess several biological properties, foremost as antioxidant and antimicrobial compounds. Several in vitro reports have described that phlorotannins showed growth inhibition and bactericidal effects against Gram+ (e.g., Bacillus cereus, Streptococcus epidermidis, Staphylococcus aureus) and Gram− bacteria (e.g., Salmonella sp., Campylobacter jejuni, Pseudomonas aeruginosa), also including antibiotic-resistant strains such as MRSA. Although the mechanisms of action of this group of compounds has not been fully elucidated, tannins could interact with membrane proteins and key metabolic enzymes, impeding bacterial growth and resulting in membrane lysis. Moreover, different phlorotannins were able to inhibit bacterial biofilm formation, production of quorum-sensing molecules, and also viral replication (e.g., influenza). Few in vivo studies support their effectiveness as antibiotics, whereas clinical trials studying other properties consistently report high bioavailability and null toxicity of phlorotannins. Considering current evidence, phlorotannins could be considered as interesting candidates for antibiotic therapy clinical trials. The diversity of these natural compounds provides a promising gateway for researchers and the pharmaceutical industry to develop novel nontoxic, cost-effective, and highly efficient antibacterial formulations with a broad scope of applications.

1. Introduction

Antibiotic resistance has become the topmost threat to public health in the 21st century, with more than 40 countries sharing reports on antimicrobial resistance, which signifies criticality [1]. As such, there is a need for alternative compounds and treatments that may function as antibiotics in order to deal with this issue. In the last decade, research on natural compounds from plant and algae sources has rapidly increased, with a great number of natural molecules characterized and described. In this context, marine algae, a traditional food and medicinal East-Asian ingredient, has proven to be an excellent source of natural molecules with numerous potential and effective applications in human health [2,3]. In specific, brown algae possess some unique natural compounds with various bioactive properties, such as polysaccharides (laminaran, fucoidan, alginate), lectins, alkaloids, or polyphenols, such as phlorotannins (PT) [4]. PT are composed of polymeric units of phloroglucinol (1,3,5-trihydroxybenzene), with molecular weights ranging between 126–650 kDa. They are classified into six major groups, according to the type of linkages between phloroglucinol units and the number of hydroxyl groups (Figure 1) [5,6]:
(i)
fucols, with aryl-aryl linkages;
(ii)
phlorethols, with aryl-ether linkages;
(iii)
fucophlorethols, with aryl-aryl and aryl-ether units;
(iv)
fuhalols, with aryl-ether linkages and additional hydroxyl groups in every third ring;
(v)
carmalols, with a dibenzodioxin moiety and derived from phlorethols;
(vi)
eckols, which possess at least one three-ring moiety with a dibenzodioxin element substituted by a phenoxyl group at C-4.
Due to their polymeric structure and number of hydroxyl groups, PT are potent free-radical scavengers and can modulate proteins and chelate metals. These capacities explain the wide range of cellular and ecological roles of phlorotannins in seaweeds. Moreover, PT are herbivore deterrents and protect against desiccation, high UVB radiation, and toxic heavy metals, acting as chelators [7,8]. These compounds have been classified as generally regarded as safe (GRAS) substances by both the Food and Drug Administration (FDA) and the European Food Safety Agency (EFSA) [9,10]. In the EU, phlorotannin-rich extracts from Ecklonia cava are approved as a “novel food” and considered safe to consume, due to an great number of studies supporting their safety [10].
Applications of PT, however, are currently limited as antioxidant cosmetic ingredients, or nutraceuticals for metabolic modulation, as there is a growing body of evidence supported by regulators, suggesting that these marine polyphenols are safe and non-toxic. In addition, several reports suggest their antimicrobial potential. Herein, the potential use of PT as antibiotic compounds based on scientific evidence is briefly reviewed.

2. Scientific Studies on Antimicrobial and Antiviral Effects of Phlorotannins

PT antimicrobial potential has mainly been studied through in vitro assays, for which screening studies made on brown algae usually employ representative nosocomial Gram+ and Gram− bacteria, such as Staphylococcus aureus, or Pseudomonas aeruginosa, which usually present antibiotic resistance (Table 1). PT extracts from Sargassum species have demonstrated varying microbial growth inhibition on P. aeruginosa, S. aureus, and also in other pathogenic species such as Vibrio parahaemolyticus and the facultative pathogen Escherichia coli [6,11,12]. The brown algae Ecklonia cava and Eisenia bicyclis are also some of the most studied algae as source of PT, since these contain eckols, such as dieckol or phlorofucofuroeckol-A. These purified compounds were reported to display inhibitory and bactericidal effects on relevant gastrointestinal pathogenic bacteria such as Campylobacter jejuni, Salmonella typhimurium, or S. typhi at concentrations below 200 μg/mL [13,14]. Moreover, these eckols have been studied to reduce or nullify antibiotic resistance in some bacterial strains. For example, phlorofucofuroeckol-A from E. bicyclis downregulated the Penicillin-binding protein 2a gene, related to methicillin resistance in S. aureus exhibiting a minimum inhibitory concentration (MIC) of 16 μg/mL [13]. Likewise, fucofuroeckol-A from the same brown alga reduced biofilm formation and virulence of Streptomycin-resistant Listeria monocytogenes, with a MIC of 16 μg/mL [14]. In addition to these results, a few reports indicate that PT may also act as antiviral agents, as phlorofucofuroeckol-A from E. cava was described to greatly inhibit various strains of influenza [15], and dieckol was described to almost nullify human immunodeficiency virus (HIV) replication [16].

3. Discussion and Future Perspectives

Evidence regarding PT as antioxidants and metabolic and inflammatory modulators is vast, with a great number of studies confirming these properties by in vivo studies and clinical trials [6,26]. However, research on their potential applications as antibiotics is still limited, mainly due to the scope of reported studies (number of PT and/or microorganisms tested) and the fact that many of such works have been focused on in vitro studies, which unfortunately may not be translated to effective results in animal models or clinical trials. Nevertheless, the reported inhibitory and bactericidal effects of these molecules, specially purified compounds (e.g., dieckol, phlorofucofuroeckol-A) should be considered effective at low concentrations. Since PT have shown antioxidant, photoprotective, and anti-inflammatory activities, these could be excellent ingredients for topical antibiotic formulations and cosmetics. Moreover, PT are reported to inhibit quorum sensing and limit biofilm formation, which suggests that these compounds could contribute to reducing topical or gut infections [11,17].
Two main factors should be considered regarding potential effectiveness of PT: (1) their generally poor bioavailability and (2) their binding effectiveness to microbial pathogens. Polyphenols and specially highly-polymerized have shown very poor bioavailability (around 5–10% are absorbed), and thus, encapsulation strategies are usually developed [5]. Notably, it has also been described that PT may act as prebiotics but research on this still appears limited, and microbiota alterations based on gut infections and changes due to PT treatment should be further explored [27]. On the other hand, it has been suggested that PTs, similarly to other polyphenols, could interact with cell membrane proteins or metabolic enzymes, precipitating them and disrupting the membrane integrity [3]. This fact was reported as the main factor liable of membrane lysis in MRSA, which also acted in synergy with methicillin [24]. Altogether, despite much needed further research, there is founding evidence suggesting the potential of PT as an effective antimicrobial and antiviral compounds, among other demonstrated properties.

Author Contributions

Conceptualization, J.E., L.C. and M.A.P.; methodology, J.E. and L.C.; validation, P.G.-P., R.P.-G., M.F.-C. and L.C.; formal analysis, J.E., C.L.-L. and L.C.; investigation, J.E., C.L.-L. and A.C.-C.; resources, F.F.S. and S.B.; data curation, P.O., L.C. and M.F.-C.; writing—original draft preparation, J.E., C.L.-L. and A.C.-C.; writing—review and editing, J.E. and L.C.; visualization, L.C., P.G.-P., R.P.-G. and P.O.; supervision, P.G.-P., R.P.-G., M.F.-C. and L.C.; project administration, M.A.P. and J.S.-G.; funding acquisition, M.A.P. and J.S.-G. All authors have read and agreed to the published version of the manuscript.

Funding

The research leading to these results was supported by MICINN supporting the Ramón y Cajal grant for M.A. Prieto (RYC-2017-22891), María Zambrano grant for R. Perez-Gregorio (CO34991493-20220101ALE481), and the FPU grant for A. Carreira-Casais (FPU2016/06135), by Xunta de Galicia for supporting the program EXCELENCIA-ED431F 2020/12, the post-doctoral grant of M. Fraga-Corral (ED481B-2019/096), and L. Cassani (ED481B-2021/152). The research leading to these results was supported by the European Union through the “NextGenerationEU” program supporting the “Margarita Salas” grant awarded to P. Garcia-Perez, and the EcoChestnut Project (Erasmus+ KA202) that supports the work of J. Echave. Authors are grateful to Ibero-American Program on Science and Technology (CYTED—AQUA-CIBUS, P317RT0003), to the Bio Based Industries Joint Undertaking (JU) under grant agreement No 888003 UP4HEALTH Project (H2020-BBI-JTI-2019) that supports the work of P. Otero and C. Lourenço-Lopes and to AlgaMar company for the collaboration. The JU receives support from the European Union’s Horizon 2020 research and innovation program and the Bio Based Industries Consortium. The project SYSTEMIC Knowledge hub on Nutrition and Food Security has received funding from national research funding parties in Belgium (FWO), France (INRA), Germany (BLE), Italy (MIPAAF), Latvia (IZM), Norway (RCN), Portugal (FCT), and Spain (AEI) in a joint action of JPI HDHL, JPI-OCEANS, and FACCE-JPI launched in 2019 under the ERA-NET ERA-HDHL (n° 696295).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Chemical structure of representative phlorotannin groups. (A) Phloroglucinol monomer; (B) Trifucol; (C) Tetraphlorethol B; (D) Pentafuhalol B; (E), Fucodiphlorethol; (F) Diphlorethohydroxycarmalol; (G) Eckol; (H) Dieckol.
Figure 1. Chemical structure of representative phlorotannin groups. (A) Phloroglucinol monomer; (B) Trifucol; (C) Tetraphlorethol B; (D) Pentafuhalol B; (E), Fucodiphlorethol; (F) Diphlorethohydroxycarmalol; (G) Eckol; (H) Dieckol.
Msf 12 00043 g001
Table 1. Antimicrobial and antiviral activity of phlorotannins extracted from marine brown algae.
Table 1. Antimicrobial and antiviral activity of phlorotannins extracted from marine brown algae.
Algae SourceCompound/ExtractMicrobial StrainsMain FindingsRef.
Sargassum fusiformeCommercial phlorotannin extractPseudomonas aeruginosa, Staphylococcus aureus, Vibrio parahaemolyticus, Aeromonas hydrophilaMIC = 97 mg/mL
Reduction of P. aeruginosa virulence and biofilm formation at 6 mg/mL
[8]
Sargassum thunbergiiPT extractVibrio parahaemolyticusMIC = 0.9 mg/mL[17]
Sargassum muticumPT extractPseodomonas aeruginosa, Escherichia coli, HSV-15 mg/mL extract achieved 43.7% inhibition in biofilm formation for P. aeruginosa and 64.3% for E. coli. EC50 (HSV-1) = 0.2 mg/mL[18]
Ascophyllum nodosumPT extractSalmonella agona, Streptococcus suis, Escherichia coliMBC (E. coli, S. agona) = 3.1 mg/mL
MBC (S. suis) = 1.56 mg/mL
[19]
Fucus serratusMBC (All) = 6.25 mg/mL
Fucus vesiculosusPT extractMRSA100 μg/mL showed a 57.6% inhibition [20]
PT extractStaphylococcus aureus, Streptococcus pneumoniae, Klebsiella pneumoniae, Pseudomonas aeruginosa20 pg/mL achieved an average 61.3% inhibition, which was higher for Gram+[21]
Ishige okamuraeDiphlorethohydroxycarmalolStaphylococcus aureus, Pseudomonas aeruginosaMBC (S. aureus) = 512 μg/m
LMBC (P. aeruginosa) = 256 μg/mL
[22]
Ecklonia cavaDieckol, 8,8′-dieckolMRSA, Bacillus cereus, Campylobacter jejuni, Escherichia coli, Streptococcus epidermidis, Salmonella typhimurium, Vibrio parahaemolyticusMBC = 0-03-0.54 μmol/mL against all strains, being C. jejuni the most susceptible[11]
Phlorofucofuroeckol AHuman Influenza H1N1, A/PR/8/34, H9N2MIC = 13.48 μg/mL[15]
DieckolHIV-137.1 μg/mL inhibited viral replication by 80%[16]
EckolMRSA, Salmonella typhimurium, S. typhi, S. paratyphi, S. gallinarium, S. enteritidisMIC = 250 μg/mL; synergy if combined with ampicillin (MIC = 150 μg/mL)[12]
Eckol, phlorofucofuroeckol-A, PT extractVHSVEC50 (eckol) = 1.97 μg/mL
EC50 (phlorofucofuroeckol-A) = 0.99 μg/mL
EC50 (PT extract) = 4.76 μg/mL
1 mg/g bw daily oral administration increased survivability of fish by >40%
[23]
Eisenia bicyclisPhlorofucofuroeckol-AMRSAMIC = 16 μg/mL; down-regulation of PBP2a conferring MR[24]
Phlorofucofuroeckol-A, fucofuroeckol-A, dioxinodehydroeckolPropionibacterium acnes, Staphylococcus aureus, Streptococcus epidermidis, Pseudomonas aeruginosaMIC = 126 μg/mL, synergistic bactericidal activity in combination with tetracycline[13]
Phlorofucofuroeckol-A, dieckolMurine norovirusMIC = 0.9 μg/mL; Phlorofucofuroeckol-A showed a higher selectivity index[25]
Fucofuroeckol-AStreptomycin-R Listeria monocytogenesMIC = 16 μg/mL[14]
Abbreviations: MIC, Minimum inhibitory concentration; MBC, Minimum bactericidal concentration; EC50, Half-maximal effective concentration; MRSA, Methicillin-resistant Staphylococcus aureus; HSV-1, Herpes simplex virus-1; VHSV, Hemorrhagic septicemia virus; PBP2a, Penicillin-binding protein 2a (PBP2a).
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Echave, J.; Lourenço-Lopes, C.; Cassani, L.; Fraga-Corral, M.; Garcia-Perez, P.; Otero, P.; Carreira-Casais, A.; Perez-Gregorio, R.; Baamonde, S.; Saa, F.F.; et al. Evidence and Perspectives on the Use of Phlorotannins as Novel Antibiotics and Therapeutic Natural Molecules. Med. Sci. Forum 2022, 12, 43. https://doi.org/10.3390/eca2022-12728

AMA Style

Echave J, Lourenço-Lopes C, Cassani L, Fraga-Corral M, Garcia-Perez P, Otero P, Carreira-Casais A, Perez-Gregorio R, Baamonde S, Saa FF, et al. Evidence and Perspectives on the Use of Phlorotannins as Novel Antibiotics and Therapeutic Natural Molecules. Medical Sciences Forum. 2022; 12(1):43. https://doi.org/10.3390/eca2022-12728

Chicago/Turabian Style

Echave, Javier, Catarina Lourenço-Lopes, Lucia Cassani, Maria Fraga-Corral, Pascual Garcia-Perez, Paz Otero, Anxo Carreira-Casais, Rosa Perez-Gregorio, Sergio Baamonde, Fermín Fernández Saa, and et al. 2022. "Evidence and Perspectives on the Use of Phlorotannins as Novel Antibiotics and Therapeutic Natural Molecules" Medical Sciences Forum 12, no. 1: 43. https://doi.org/10.3390/eca2022-12728

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