Научная статья на тему 'Antimicrobial activity of surfactants of microbial origin'

Antimicrobial activity of surfactants of microbial origin Текст научной статьи по специальности «Биологические науки»

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Biotechnologia Acta
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MICROBIAL LIPOPEPTIDES / RHAMNOLIPIDS AND SOPHOROLIPIDS / ANTIBACTERIAL AND ANTIFUNGAL ACTIVITY / МіКРОБНі ЛіПОПЕПТИДИ / РАМ НОЛі ПіДИ ТА СОФОРОЛіПіДИ / АНТИБАКТЕРіАЛЬНА ТА АНТИФУНГАЛЬНА АКТИВНіСТЬ / МИКРОБНЫЕ ЛИПОПЕПТИДЫ / РАМНОЛИПИДЫ И СОФОРОЛИПИДЫ / АНТИБАКТЕРИАЛЬНАЯ И АНТИФУНГАЛЬНАЯ АКТИВНОСТЬ

Аннотация научной статьи по биологическим наукам, автор научной работы — Pirog T.P., Lutsay D.A., Kliuchka L.V., Beregova K.A.

The recent literature data about the antibacterial and antifungal activity of microbial surfactants (lipopeptides synthesized by representatives of genera Bacillus, Paenibacillus, Pseudomonas, Brevibacillus, rhamnolipids of bacteria Pseudomonas, Burkholderia, Lysinibacillus sp., sophorolipids of yeasts Candida ( Starmerell a) and Rhodotorula ), and our own experiments data concerning antimicrobial activity of surfactants synthesized by Acinetobacter calcoaceticus IMB B-7241, Rhodococcus erythropolis IMB Aс-5017 and Nocardia vaccini IMV B-7405 were presented. The analysis showed that lipopeptides were more effective antimicrobial agents compared to glycolipids. Thus, the minimum inhibitory concentrations (MIC) of lipopeptides, ramnolipids and sophorolipids are on average (μg/ml): 1-32, 50-500, and 10-200, respectively. The MIC of surfactants synthesized by the IMV B-7241, IMV Ac-5017 and IMV B-7405 strains are comparable to those of the known microbial lipopeptides and glycolipids. The advantages of glycolipids as antimicrobial agents compared with lipopeptides were the possibility of their synthesis on industrial waste and the high concentration of synthesized surfactants. The literature data and our own results indicate the need to study the influence of microbes’ cultivation conditions on the antimicrobial activity of the final product.

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АНТИМИКРОБНАЯ АКТИВНОСТЬ ПОВЕРХНОСТНО-АКТИВНЫХ ВЕЩЕСТВ МИКРОБНОГО ПРОИСХОЖДЕНИЯ

Целью работы был анализ данных литературы последних лет относительно антибактериальной и антифунгальной активности микробных поверхностно-активных веществ (ПАВ) (липопептидов, синтезированных представителями родов Bacillus, Paenibacillus, Pseudomonas, Brevibacillus, рамнолипидов бактерий родов Pseudomonas, Burkholderia, Lysinibacillus, софоролипидов дрожжей родов Candida ( Starmerella и Rhodotorula ), а также собственных экспериментальных исследований антимикробной активности ПАВ, синтезированных Acinetobacter calcoaceticus ІМВ В-7241, Rhodococcus erythropolis ІМВ Aс-5017 и Nocardia vaccinii ІМВ В-7405. Проведенный анализ показал, что липопептиды являются более эффективными антимикробными агентами по сравнению с гликолипидами. Минимальные ингибирующие концентрации (МИК) липопептидов, рамнолипидов и софоролипидов составляют в среднем (мкг/мл): 1-32, 50-500 и 10-200 соответственно. МИК поверхностно-активных веществ, синтезированных штаммами ІМВ В-7241, ІМВ Ас-5017 и ІМВ В-7405, находятся в пределах, установленных для известных липопептидов и гликолипидов. Преимуществами гликолипидов как антимикробных агентов по сравнению с липопептидами являются возможность их синтеза на промышленных отходах и высокая концентрация синтезированных ПАВ. Немногочисленные данные литературы и собственные результаты авторов свидетельствуют о необходимости проведения исследований влияния условий культивирования продуцентов на антимикробную активность целевого продукта.

Текст научной работы на тему «Antimicrobial activity of surfactants of microbial origin»

UDC 759.873.088.5:661.185 https://doi.org/10.15407/biotech12.01.039

ANTIMICROBIAL ACTIVITY OF SURFACTANTS

OF MICROBIAL ORIGIN

T. P. PIROG, D. A. LUTSAY, L. V. KLIUCHKA, K. A. BEREGOVA

National University of Food Technologies, Kyiv, Ukraine E-mail: tapirog@nuft.edu.ua

Received 17.08.2018 Revised 21.12.2018 Accepted 14.01.2019

The recent literature data about the antibacterial and antifungal activity of microbial surfactants (lipopeptides synthesized by representatives of genera Bacillus, Paenibacillus, Pseudomonas, Brevibacillus, rhamnolipids of bacteria Pseudomonas, Burkholderia, Lysinibacillus sp., sophorolipids of yeasts Candida (Starmerella) and Rhodotorula), and our own experiments data concerning antimicrobial activity of surfactants synthesized by Acinetobacter calcoaceticus 1MB B-7241, Rhodococcus erythropolis 1MB Ac-5017 and Nocardia vaccini IMV B-7405 were presented. The analysis showed that lipopeptides were more effective antimicrobial agents compared to glycolipids. Thus, the minimum inhibitory concentrations (MIC) of lipopeptides, ramnolipids and sophorolipids are on average (pg/ml): 1-32, 50-500, and 10-200, respectively. The MIC of surfactants synthesized by the IMV B-7241, IMV Ac-5017 and IMV B-7405 strains are comparable to those of the known microbial lipopeptides and glycolipids. The advantages of glycolipids as antimicrobial agents compared with lipopeptides were the possibility of their synthesis on industrial waste and the high concentration of synthesized surfactants. The literature data and our own results indicate the need to study the influence of microbes' cultivation conditions on the antimicrobial activity of the final product.

Key words: microbial lipopeptides, rhamnolipids and sophorolipids, antibacterial and antifungal activity.

Biodegradation and non-toxic microbial surfactants are used in many fields due to their surface active and emulsifying properties, antimicrobial and antiadhesive activity. They are a useful alternative to standard chemical surfactants in various industrial, medical and nature conservation technologies [1-3].

Microbial surfactant research has a long history. In 1968 it was found that Bacillus subtilis AMS-H2O-1 could produce surfactin [4], in 1977 B. subtilis DS-104 was shown to produce iturin [5], and the first reports of rhamnolipids came from as early as 1940's [6], while their bactericidal properties were discovered in early 1970's [7]. However, despite this, the detailed studies of their antimicrobial properties commenced quite recently.

In 1997, Vollenbroich et al. established that the linopeptide produced by B. subtilis

OKB105 at 0.032 mg/ml inhibits the growth of Mycoplasma hyorhinis and Mycoplasma orale, which can cause inflectional disease of the urinary tract. This was the first research into the antimicrobial action of that surfactin [8].

In 2001, Abalos et al. revealed antifungal action of seven homologues of rhamnolipids of Pseudomonas aeruginosa AT10, which at low concentrations (16-32 pg/ml) inhibited growth of fungi belonging to the genera Aspergillus, Penicillium, Aureobasidium, and of the phytopathogens Botrytis and Rhizoctonia [9].

In 2003, the rhamnolipids of P. aeruginosa 47T2 NCBIM 40044 were shown to have antibacterial properties [10]. Thus, minimal inhibiting concentrations (MIC) of these surfactants against some bacteria of the genera Serratia, Enterobacter, Klebsiella, Staphylococcus were 0.5-32 pg/ml. Reports [8-10] were the impulse for further research

of the antimicrobial action of microbial surfactants [11-13].

One reason for such interest to microbial surfactants as antimicrobial agents is the pathogen resistance to widespread antibiotics and chemical biocides [11, 13].

Compared to the well-known antimicrobial compounds, microbial surfactants have a number of advantages [1, 2, 11, 13]. They are biodegradable and non-toxic, which prevents environmental pollution and allergies. They can be implemented in a wide range of pH, temperature and other environmental factors, due to their stable physical and chemical properties. Also, their action mechanism is based on the disruption of the cytoplasmic membrane, decreasing the possibility of microorganism resistance [5, 8, 10, 11].

The high interest to the microbial surfactants is evidenced by the many publications about these products of microbial synthesis. A few literature reviews were published in the last five years on the properties and perspectives of the practical implementation of microbial surfactants [1, 3, 14-19]. Those reviews mostly focused on certain surfactant types (rhamnolipids, lipopeptides, sophorolipids etc.) with emphasis on certain properties of these compounds. For example, Zhao et al. [17] pay attention mostly to the anti-inflammatory, antitumour, antiviral, and antiplatelet properties of lipopeptides, their interaction with biofilms, while the antibacterial effect is not considered at all and the antifungal is discussed briefly. The review [15] provides not only the specifics of the chemical composition but also the information about antimicrobial activity of lipopeptides, but the information is of almost a ten years ago. Similarly, Cortes-Sanchez Ade et al. [14], while analyzing antimicrobial properties of glycolipids, largely refer to the data of 2005-2010.

This review aims to summarize literature of the last several years on the antimicrobial potential of various surfactant substances of microbial origin.

Lipopeptides of Bacillus sp. as antimicrobial agents

The bacteria of the genus Bacillus are among the most studied sources of lipopeptides. The lipopeptydes are grouped into three families of cyclic compounds: surfactin, iturin and fengicin, differing in the number and sequence of the amino acids they include, as well as in the length of the acyl chain [15, 16]. Differences in the chemical composition

and construction determine the range of their biological action. Thus, iturin and fengicin have antifungal properties while surfactin with a shorter acyl chain is characterized by a wider range of antibacterial action [15, 16].

Antibacterial action. In 2015, Torres et al. [20] established antimicrobial activity of the surfactant complex of Bacillus subtilis subsp. subtilis CBMDC3f, which contains four surfactin homologues and one for each iturin and fengicin. When the complex was added to cell suspension of Listeria monocytogenes 01/155 at 0.5 mg/ml, the number of viable cells dropped two orders of magnitude after 25 minutes. A similar effect towards Bacillus cereus MBC1 and Staphylococcus aureus ATCC 29213 was seen at higher concentrations of lipopeptide complex (1-2 mg/ml). The authors state that surfactants of similar composition produced by other strains of Bacillus licheniformis or B. subtilis were active only against B. cereus and S. aureus, without antagonistic activity against the genus Listeria [20].

Sharma et al. [21] studied antimicrobial activity of lipopeptides produced by Bacillus pumilus DSVP18 on potato peel substrate. Minimum inhibiting concentration against B. cereus MTCC 430, Escherichia coli MTCC 1687, Salmonella enteritidis MTCC 3219, and that against S. aureus MTCC 5021 was 30 ug/ml.

Surfactin of Bacillus amyloliquefaciens ST34 showed antimicrobial activity against a range of both Gram-negative (Escherichia coli ATCC 13706, Salmonella typhimurium ATCC 14028, Klebsiella pneumoniae ATCC 10031, Serratia sp. SM14, Enterobacter sp. E11) and Gram-positive (B. cereus ST18, Enterococcus sp. C513, Micrococcus sp. AQ4S2, S. aureus C2) bacteria [22]. At the concentration of surfactin 0.26 mg/ml, zones of bacterial growth inhibition were 13-17 mm.

Chen et al. [23] isolated from the sediments of Bohai Sea a strain of Bacillus licheniformis MB01 which produces a complex of surfactin and fatty acids showing antibacterial activity against E. coli, Vibrio cholerae, Vibrio parahaemolyticus, Vibrio harveyi, Pseudomonas aeruginosa, S. aureus, Proteus species. For example, its MIC against V. рarahaemolyticus was 50 ug/ml [23].

Strain B. subtilis SK.DU4 synthesizes the complex of bacteriocin-like peptide and iturin-like lipopeptide with 15 carbon atoms in the acyl chain [24]. The bacteriocin-like peptide had antimicrobial action against Micrococcus luteus MTCC106 and Listeria monocytogenes

MTCC839 (growth inhibition zone 12 and 14 mm, respectively). If only the inturin-like lipopeptide was present, the zone of growth inhibition was 11 mm in both test cultures. If the mixture of bacitracin and lipopeptide was used, the zone of M. luteus MTCC106 and L. monocytogenes MTCC839 growth inhibition increased to 15 and 17 mm, respectively.

The study of Zhou et al. [25] is one of the first concerning dependence of surfactin antimicrobial activity on the carbon source in the culture medium of B. subtilis HH2, as well as the stability of antimicrobial action in a wide range of temperature (60-121 °С), pH (1-12), and in the presence of trypcin (100-300 pg/ml, pH 8) and pepsin (100-300 pg/ml, pH 2). It was found that surfactin synthesized on a mixture of glucose (0.33 %) and cellulose (0.67 %) had higher antimicrobial activity (at 0.4 mg/ml surfactin, the growth inhibition zones of E. coli CCTCC AB 212358 and S. aureus CCTCC AB 91053 were 16 and 14 mm, respectively). Lipopeptide obtained on medium with 1 % glucose, had low antimicrobial effect. Antimicrobial activity of surfactin remained constant at 60-100 °С, pH 2-11, and in the presence of trypsin and pepsin.

Due to synthesis of surfactin, bacteria of the genus Bacillus are considered promising in controlling the growth of such phytopathogens as P. syringae (causes root infection of arabidopsis), Xanthomonas axonopodis pv. glycines (bacterial pustule of soybean), and phytopathogen mycoplasms Spiroplasma citri and Acholeplasma laidlawii, which cause etiolation in citruses, clover phyllody and phytoplasma disease in solanaceous crops, respectively [15, 16].

B. subtilis 9407 synthesizes the complex of lipopeptides, the main one being C13-C16 surfactin A [26]. This complex showed of the antimicrobial effect against Acidovorax citrulli MH21 the causative agent of pumpkin bacterial blotch (growth inhibition zone 18 mm). To prove the role of surfactin in inhibition this pathogen, the authors obtained a mutant strain unable of synthesize lipopeptide. The mutant had no antimicrobial activity. Besides A. dtrulli MH21, lipopeptides of strain 9407 showed antimicrobial effect on other phytopathogenic bacteria: Pseudomonas syringae pv. tomato DC3000, Хanthomonas campestris pv. campestris Xcc 8004, Pectobacterium carotovora subsp. carotovora Ecc 09, Pectobacterium atrosepticum SCRI1043 (growth inhibition zones 10-18 mm) [26].

In 2018 [27] was reported about a sea isolate Bacillus pumilus SF214 wich produced pumilacidin (the mixture of cyclic heptapeptides linked to fatty acids of different lengths). The lipopeptide inhibited S. aureus ATCC 6538 (in the presence of supernatant, growth inhibition zone was 10 mm.

Antifungal activity. In the publications on the antifungal activity pay the most attention to the effect of these surfactants on phytopathogenic fungi. Since we provided the information on antifungal effect of lipopeptides produced by rhizosphere and endophytic bacteria of the genus Bacillus, which are promising for control the number of phytopathogenic fungi, what we reported in the review [28], we shall now pay attention to studies which have appeared after then. The lipopeptide antifungal activity is determined by analyzing such parameters as MIC [29-34], degree of the fungal growth inhibition [35, 36], and the diameter of fungal growth inhibition zone [37].

The data on MIC of lipopeptides produced by bacteria of the genus Bacillus against fungi and yeast are summarized in Table 1. According to the data, the highest antifungal activity is shown for B. subtilis RLID 12.1 lipopeptides. MIC against yeasts of the genera Cryptococcus and Candida was only 1-20 pg/ml, that orders of magnitude lower than MIC of other lipopeptides against fungi. Notably, the antimicrobial activity of lipopeptides of Bacillus sp. AR2 depends on the carbon source in the culture medium [20]. The strain AR2 was found to produce the mixture of homologues of iturin, fengicin and surfactin. If the strain was grown in medium with sucrose, glycerol, sorbitol and maltose the prevailing fraction in the complex was C15 surfactin. However the most active antifungal agents were lipopeptides produced on sucrose. Sarwar et al. [35] studied the degree of growth inhibition of phytopathogenic fungi Fusarium moniliforme KJ719445, Fusarium oxysporum (the strain was not specified), Fusarium solani SAN1077, Trichoderma atroviride P150907 for the action of lipopeptides synthesized by bacteria of the genus Bacillus.

It was found that lipopeptides of B. amyloliquefaciens FZB42, B. subtilis NH-100 and B. subtilis NH-217 inhibited fungal growth by 83-87, 79-80, and 76-79% respectively.

Lipopeptides synthesized by Bacillus XT1 CECT 8661 added at 2-10 mg/ml inhibited the growth of Botrytis cinerea by 19-72%, and maximum degree of inhibition

Table 1. Minimum inhibitory concentrations of Bacillus sp. lipopeptides against fungi

Test culture Lipopeptide producer MIC, ^g/ml References

Genus Species, strain

Alternaria Alternaria solani Bacillus subtilis CU 12 150 [30]

Alternaria alternata MTCC 2724 Bacillus sp. AR2 500-750* [34]

Alternaria citri MTCC 4875 Bacillus sp. AR2 500-750* [34]

Fusarium Fusarium oxysporum f. sp. iridacearum Bacillus subtilis BBG125 10 [33]

Fusarium sambucinum Bacillus subtilis CU 12 100 [30]

Fusarium solani ATCC 36031 Bacillus sp. AR2 250-750* [34]

Fusarium oxysporum MTCC 7229 Bacillus sp. AR2 250-750* [34]

Fusarium solani Bacillus subtilis SPB1 3000 [31]

Rhizoctonia Rhizoctonia bataticola Bacillus subtilis SPB1 40 [32]

Rhizoctonia solani Bacillus subtilis SPB1 4000 [32]

Rhizopus Rhizopus stolonifer Bacillus subtilis CU 12 100 [30]

Verticillium Verticillium dahliae Bacillus subtilis CU 12 100 [30]

Cladosporium Cladosporium cladosporioides ATCC 16022 Bacillus sp. AR2 750-2000* [34]

Scopulariopsis Scopulariopsis acremonium ATCC 58636 Bacillus sp. AR2 125-500* [34]

Microsporum Microsporum gypseum MTCC 4522 Bacillus sp. AR2 125-500* [34]

Trichophyton Trichophyton rubrum MTCC 2961 Bacillus sp. AR2 750-2000* [34]

Botrytis Botrytis cinerea Bacillus XT1 CECT 8661 8000 [36]

Cryptococcus Cryptococcus spp. Bacillus subtilis RLID 12.1 1-16 [29]

Candida Candida spp. Bacillus subtilis RLID 12.1 2-20 [29]

Note.* — different MIC values dependent on the carbon source in the culture medium.

was seen at the highest studied surfactant concentration [36].

For the action surfactin of B. amylolique-faciens ST34 at concentration 0.26 mg/ml, growth inhibition zones in different strains of Candida albicans and Cryptococcus neoformans were in the range of 13-15 mm [22].

In our review [28] we reported an increased synthesis of antifungal lipopeptides (in particular, fengicin and iturin) in response to the presence of phytopathogenic fungi in the medium of producer cultivation. Zihalirwa Kulimushi et al. [37] studied the effect of a lipopeptide complex (surfactin, fengicin and iturin) produced by B. amyloliquefaciens S499 on the phytopathogenic fungus Rhizomucor variabilis, and the possibility of inducing the antifungal compounds synthesis in the presence of a pathogen in the culture medium of strain S499. Experiments showed that co-culturing B. amyloliquefaciens S499 and Rhizomucor variabilis led to an almost three-

fold increase in fengicin content and increased the antifungal effect [37].

The another interesting research [38] showed that Bacillus amyloliquefaciens UCMB5113 syntesized the mixture of linear fengicins, whereas they commonly occur only in the cyclic form [15, 16]. Linear fengicins were divided into 14 fractions, all fractions showed antagonistic activity against Alternaria brassicicola, Alternaria brassicae, Botrytis cinerea, Sclerotinia sclerotiorum and Verticillium longisporum; but the fraction 9 had the highest antifungal effect. According to the analysis, it belonged to the family of C15-fengicin. The authors suppose that all other fractions have shorter acyl chains and so are less active.

Antimicrobial effect of lipopeptides produced by other microorganisms

Representatives of the genera Paeni-bacillus [16, 39-41], Pseudomonas [42-46],

Brevibacillus [47], Corynebacterium [48], Aneurinibacillus [49], Streptomyces [50], even Propionibacterium [51], Citrobacter and Enterobacter [52] also synthesises lipopeptides.

High antimicrobial activity was revealed for lipopeptide surfactants of strain Paenibacillus sp. MSt1, isolated from the peat beds of tropical forests. Thus, its MIC was (pg/ml) 1.5 against E. coli ATCC 25922; 25 — methicillin resistant strain S. aureus ATCC 700699, and 12.5 — C. albicans IMR [39].

Huang et al. [40] established high antimicrobial activity of paenibacterin of Paenibacillus thiaminolyticus OSY-SE. MIC of the lipopeptide against strains E. coli, P. aeruginosa, Acinetobacter baumannii, K. pneumoniae, S. aureus and E. faecalis were fairly low: 8-16 pg/ml, comparable to the MIC of such antibiotics as polymixin B and vancomycin.

In 2017, was reported about strain Paenibacillus sp. OSY-N that produce the mixture of lipopeptides BMY-28160, permetin А, a novel cyclic lipopeptide and its linear analogues (paenipeptins А, В and С) [41]. Differences in the compound content underlie their different biological effect. Thus far, the highest antimicrobial effect was seen in paenipeptin С (contains C8-acyl chain and isoamino acid): MIC against Grampositive (B. cereus ATCC 11778, Listeria innocua ATCC 33090, S. aureus ATCC 25923, S. aureus ATCC 6538) and Gram-negative (E. coli K-12, E. coli ATCC 25922, Salmonella enterica ser. Typhimurium LT2, S. enterica ser. Typhimurium LT2) bacteriae were 2-4 and 0.5-2 pg/ml, respectively. The authors explain such activity of paenipeptin С, unlike other lipopeptides, by a longer acyl chain, and presence of unusual amino acids and their conformation.

Although bacteria of the genus Pseudomonas are more known as sources of glycolipids [1, 2, 7, 9, 10, 12, 14], there are data on their ability to produce lipopeptides, too. As early as 1970's the structure of lipopeptide viscosin was established (the compound was produced by Pseudomonas fluorescens), with antimicrobial effect [42] of such magnitude that intensive research of its biological properties lasted until 2000's [43]. Currently, viscosin has been established to have an antimicrobial effect against 94 Gramnegative and 72 Gram-positive bacteria and 95 fungal species [44].

Ma et al. [45] established that Pseudomonas sp. CMR5C produced orfamide B and G, with the same amino acid sequence but different

acyl chain lenth: C14 for orfamide B and C16 for orfamide G. Irrespectively of the acyl chain length, orfamide had no antifungal effect against Magnaporthe oryzae VT5M1, however at 50 pmole/ml the appressorium of M. oryzae VT5M1 did not develop.

Pseudomonas aeruginosa МА-1 grown on olive oil (4 % ) produced lipopeptides in the high concentration of 12.5 g/l [46] of low antimicrobial effect; the growth inhibition zone of S. aureus ATCC 43300 did not exceed 7-9.5 mm at surfactant concentration of 0.5-5 g/l.

The lipopeptide brevibacillin (produced by Brevibacillus laterosporus OSY-I1) has high antimicrobial effect on Gram-positive bacteria (MIC 2-4 pg/ml) [47]. Notably, its MIC for Gram-negative bacteriae was higher than 32 pg/ml.

Dalili et al. [48] studied the antimicrobial effect of coryxin, produced by Corynebacterium xerosis NS5 [48]. It was found that coryxin had low antimicrobial activity against Gram-negative bacteria (MIC for strains E. coli and P. aeruginosa were 3120 and 10 000 pg/ml, respectively). However, MIC of this lipopeptides against Gram-positive bacteria S. aureus and Streptococcus mutans were significantly lower (190 pg/ml).

The aneurinifactin, produced by sea bacteria Aneurinibacillus aneurinilyticus SBP-11 A, had significantly higher antimicrobial activity compared to coryxin [49]. Its MIC against strains E. coli MTCC 443 and S. aureus MTCC 96 was 8 pg/ml, and P. aeruginosa MTCC — 16-424 pg/ml.

The study [50] described the lipopeptide produced by Streptomyces amritsarensis sp. MTCC 11845T, which at 10 pg/ml showed antibacterial activity to Gram-positive bacteria. The growth inhibition zones for B. subtilis MTCC 619, Staphylococcus epidermidis MTCC 435 and Mycobacterium smegmatis MTCC 6 were 21, 17, 15 mm, respectively. Meanwhile there was no antimicrobial activity to Gram-negative bacteria and fungi, perhaps because of a short (С12) acyl chain of the lipopeptide.

While bacteria of the genus Propioni-bacterium are known sources of organic acids and vitamins, recent research [51] established that Propionibacterium freudenreichii subsp. freudenreichii PTCC 1674 produces the lipopeptide surfactant inhibiting Rhodococcus erythropolis and B. cereus: MIC for both was 25 mg/ml.

Strains Citrobacter sp. S-3, S-6 and S-7, Enterobacter sp. S-4, S-5, S-9 S-10, S-11 and

S-12 were isolated from polluted soil. They [52] produced the complex of lipopeptides with antimicrobial effect to Gram-positive and Gram-negative bacteria. The strains S-3 and S-11 were shown to produce fractions Fr-c and Fr-e with P-hydroxy fatty acids of chain length С14 and С17, respectively. Thus they can be classified as belonging to the fengicin and iturin families. However the antimicrobial effect was seen only in the purified lipopeptide fraction Fr-c with the shorter acyl chain. Its MIC were 12, 15 and 16 ug/ml against Gram-positive test cultures Micrococcus luteus MTCC106, S. aureus MTCC1430 and S. epidermidis MTCC435, and 20 and 32 ug/ml against Gram-negative test cultures Serratia marcescens and P. aeruginosa ATCC27853, respectively. Notably no of all lipopeptides had an antifungal effect on C. albicans MTCC1637.

A summary of lipopeptides antibacterial activity is shows in Table 2, composed to compare MIC of different lipopeptides for the same test cultures. The lipopeptides produced by bacteria of the genus Paenibacillus showed the highest antimicrobial activity, a moderate activity — surfactants of the genus Bacillus, and lipopeptides of such atypical producer as Corynebacterium and Propionibacterium were not active enough.

According to recent literature, the antimicrobial activity of lipopeptides depends on their content and on the test culture (species and strain). Usually, higher antifungal activity is seen in lipopeptides with longer (С16-С18) acyl chains, and compounds with fewer carbons atoms (С7-С14) in the fatty acid chain have antibacterial effect. However, currently there is not enough information in the literature, on the basis of which it would be possible to do correct conclusions about the influence of the chemical composition of lipopeptides on their antimicrobial activity. Table 2 contains more higher MIC of lipopeptides than previously described [15, 16], perhaps because the reported data [15, 16] are given for individual substances but not for the complexes analyzed in our review.

Antimicrobial activity of rhamnolipids

A glycolipids has a carbohydrate part which might be rhamnose, trehalose, sophorose etc., and a lipid chain. Accordingly, they are classified into rhamno- trehaloso-, sophorolipids, etc. [1, 2, 14, 18, 53]. Currently, rhamnolipids are the most studied of them. Only in the last few years there were published several reviews [54-60] dedicated to the increasing rhamnolipid biosynthesis, new

avenues and problems of their application in various industrial and medical practices.

In a rhamnolipids, one or two rhamnoses are bound to one, two or seldom three molecules of P-hydroxyalyphatic acids. Depending on the number of carbohydrate and fatty acid molecules, the rhamnolipids can be grouped into mono-rhamno-mono-lipids, mono-rhamno-di-lipids, di-rhamno-mono-lipids and di-rhamno-di-lipids [58, 60]. Over sixty rhamnolipid homologues are produced by microorganisms of the genus Pseudomonas (P. chlororaphis, P. alcaligenes, P. putida, P. stutzeri, etc.), and strains of P. aeruginosa are the main rhamnolipid sources. Lately, there were reports of rhamnolipid-synthesizing abilities in bacteria of the genera Acinetobacter (A. calcoaceticus), Enterobacter, Pantoea, Burkholderia, Myxococcus [58-60].

The effect of rhamnolipid on bacteria

According to Tedesco et al., rhamno-lipids are probably produced by many microorganisms [61]. The rhamnolipid-producing strains of microbiota belonging to Psychrobacter, Arthrobacter and Pseudomonas were isolated from the Ross Sea (Antarctica). Monorhamnolipids at concentration 1 mg/ml inhibited the growth of pathogenic strains of Burkholderia (Table 3). Given the high antimicrobial activity of rhamnolipids of Pseudomonas BTN 1, the next step was separation of the rhamnolipid complexes into fractions. This yielded three kinds of monorhamnolipids with different lipid chain length. For each fraction, the researchers were determined the minimum inhibitory and minimum bactericidal concentrations (MBC).

The fractions 1 and 2 of monorhamnolipids with shorter acyl chains were most active. Thus, MIC of these fractions against

B. cenocepacia LMG 16656, B. metallica LMG 24068, B. seminalis LMG 24067, B. latens LMG 24064 and S. aureus 6538P were about 1.56-12.5 pg/ml, and MBC did not exceed 200 pg/ml.

Chebbi et al. [62] isolated from engine oil-polluted soil the strain P. aeruginosa W10, which produced 9.7 g/l rhamnolipids on a medium with 2% glycerol. However, the antimicrobial effect of the surfactants turned out to be relatively low. Thus, MIC of rhamnolipid complex of strain W10 against the pathogenic strains E. coli ATCC 25922, S. aureus (MRSA) ATCC 43300 and

C. albicans ATCC 10231 were 37.50, 9.37 and 2.34 mg/ml, respectively.

The effect of mono- and dirhamnolipids produced by Burkholderia thailandensis

Table 2. Antibacterial activity of lipopeptides against some microorganisms

Test culture Lipopeptide source MIC, ^g/ml References

Escherichia coli O157:H7 ATCC 43889 Paenibacillus sp. OSY-N (paenipeptin C) 0.5-1 [39]

Escherichia coli ATCC 25922 Paenibacillus sp. OSY-N (paenipeptin C) 0.5-1 [39]

Paenibacillus sp. MSt1 1.5 [37]

Paenibacillus thiaminolyticus OSY-SE 8 [38]

Escherichia coli O157:H7 EDL 933 Paenibacillus sp. OSY-N (paenipeptin C) 0.5-1 [39]

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Paenibacillus thiaminolyticus OSY-SE 8 [38]

Bacillus laterosporus OSY-I1 32 [40]

Escherichia coli 2276 Paenibacillus thiaminolyticus OSY-SE 8 [38]

Escherichia coli MTCC 443 Aneurinibacillus aneurinilyticus SBP-11 8 [42]

Escherichia coli K-12 Paenibacillus sp. OSY-N (paenipeptin C) 0.5 [39]

Bacillus laterosporus OSY-I1 >32 [40]

Escherichia coli MTCC 1687 Bacillus pumilus DSVP18 30 [21]

Escherichia coli* Corynebacterium xerosis NS5 3120 [39]

Staphylococcus aureus (methicillin-resistant) Bacillus laterosporus OSY-I1 1 [40]

Staphylococcus aureus ATCC 6538 Bacillus laterosporus OSY-I1 1-2 [40]

Staphylococcus aureus ATCC 25923 Paenibacillus sp. OSY-N (paenipeptin C) 2-4 [39]

Staphylococcus aureus ATCC 6538 Paenibacillus sp. OSY-N (paenipeptin C) 4-8 [39]

Staphylococcus aureus (methicillin-resistant) Paenibacillus sp. OSY-N (paenipeptin C) 8 [39]

Staphylococcus aureus MTCC 96 Aneurinibacillus aneurinilyticus SBP-11 8 [42]

Staphylococcus aureus (methicillin-resistant) Enterobacter sp. S-11 15 [44]

Staphylococcus epidermidis* Enterobacter sp. S-11 16 [44]

Staphylococcus aureus ATCC 700699 Paenibacillus sp. MSt1 25 [37]

Staphylococcus aureus MTCC 5021 Paenibacillus sp. OSY-N (paenipeptin C) 16-32 [39]

Paenibacillus thiaminolyticus OSY-SE 32 [38]

Bacillus pumilus DSVP18 30-35 [21]

Staphylococcus aureus ATCC 43300 Paenibacillus thiaminolyticus OSY-SE 32 [38]

Staphylococcus aureus* Corynebacterium xerosis NS5 190 [41]

Bacillus cereus ATCC 11778 Bacillus laterosporus OSY-I1 2-4 [40]

Paenibacillus sp. OSY-N (paenipeptin C) 4 [39]

Bacillus cereus ATCC 14579 Bacillus laterosporus OSY-I1 1,0 [40]

Paenibacillus sp. OSY-N (paenipeptin C ) 8 [39]

Bacillus cereus MTCC 430 Bacillus pumilus DSVP18 30-35 [21]

Bacillus cereus* Propionibacterium freudenreichii subsp. freudenreichii PTCC 1674 25 000 [43]

Bacillus subtilis MTCC 619 Aneurinibacillus aneurinilyticus SBP-11 16 [42]

Listeria monocytogenes OSY-8578h Bacillus laterosporus OSY-I1 1-2 [40]

Table 2. Continued

Test culture Lipopeptide source MIC, ^g/ml References

Listeria innocua ATCC 33090 Bacillus laterosporus OSY-I1 1-2 [40]

Paenibacillus sp. OSY-N (paenipeptin C) 2-4 [39]

Listeria monocytogenes Scott A Bacillus laterosporus OSY-I1 1 [40]

Paenibacillus thiaminolyticus OSY-SE 2 [38]

Paenibacillus sp. OSY-N (paenipeptin C) 4-8 [39]

Pseudomonas aeruginosa ATCC 27853 Paenibacillus sp. OSY-N (paenipeptin C) 1-2 [39]

Paenibacillus thiaminolyticus OSY-SE 8 [38]

Bacillus laterosporus OSY-I1 >32 [40]

Pseudomonas aeruginosa ATCC 999 Paenibacillus thiaminolyticus OSY-SE 8 [38]

Pseudomonas aeruginosa ATCC 2325 Paenibacillus thiaminolyticus OSY-SE 8 [38]

Pseudomonas aeruginosa MTCC 424 Aneurinibacillus aneurinilyticus SBP-11 16 [42]

Pseudomonas aeruginosa* Enterobacter sp. S-11 30 [44]

Pseudomonas aeruginosa* Corynebacterium xerosis NS5 10 000 [41]

Klebsiella. pneumoniae 2461 Paenibacillus thiaminolyticus OSY-SE 4 [38]

Klebsiella pneumoniae MTCC 7162 Aneurinibacillus aneurinilyticus SBP-11 4 [42]

Klebsiella pneumoniae 2463 Paenibacillus thiaminolyticus OSY-SE 8 [38]

Klebsiella pneumoniae ATCC 700603 Paenibacillus thiaminolyticus OSY-SE 8 [38]

Klebsiella pneumoniae 2317 Paenibacillus thiaminolyticus OSY-SE 64 [38]

Enterococcus faecalis ATCC 51299 Enterococcus faecalis 2731 Bacillus laterosporus OSY-I1 Paenibacillus thiaminolyticus OSY-SE 4-8 8 [40] [38]

Enterococcus faecalis ATCC 29212 Enterococcus faecalis ATCC 700802 Paenibacillus thiaminolyticus OSY-SE 16 [38]

Paenibacillus sp. OSY-N (paenipeptin C) Paenibacillus thiaminolyticus OSY-SE 32 64 [39] [38]

Salmonella enterica ser. Typhimuri-um LT2 Paenibacillus sp. OSY-N (paenipeptin C) 0.5-1 [39]

Salmonella enterica ser.Typhimuri-um DT104 Paenibacillus sp. OSY-N (paenipeptin C) 0.5-1 [39]

Salmonella enteritidis MTCC 3219 Bacillus pumilus DSVP18 30-35 [21]

Salmonella typhimurium DT 109 Bacillus laterosporus OSY-I1 >32 [40]

Acinetobacter baumannii ATCC BAA-747 Paenibacillus thiaminolyticus OSY-SE 2 [38]

Acinetobacter baumannii 2315 Paenibacillus thiaminolyticus OSY-SE 2 [38]

Alicyclobacillus acidoterrestris ATCC49025 Bacillus laterosporus OSY-I1 0.5-1 [40]

Alicyclobacillus acidoterrestris Bacillus laterosporus OSY-I1 1 [40]

Streptococcus agalactiae* Paenibacillus sp. OSY-N (paenipeptin C) 0.5-1 [39]

Streptococcus mutans* Corynebacterium xerosis NS5 25 000 [41]

Lactobacillus plantarum ATCC 8014f Bacillus laterosporus OSY-I1 1 [40]

Table 2. Continued

Test culture Lipopeptide source MIC, ^g/ml References

Lactococcus lactis ATCC 11454g Bacillus laterosporus OSY-I1 2 [40]

Clostridium difficile A515c Bacillus laterosporus OSY-I1 4-8 [40]

Rhodococcus erythropolis* Serratia marcescens* Propionibacterium freudenreichii subsp. freudenreichii PTCC 1674 Enterobacter sp. S-11 25 000 20 [43] [44]

Vibrio cholerae MTCC 3906 Aneurinibacillus aneurinilyticus SBP-11 16 [42]

Vibrio parahaemolyticus* Bacillus licheniformis MB01 50 [23]

Micrococcus luteus* Enterobacter sp. S-11 12 [44]

Enterobacter aerogenes* Paenibacillus sp. OSY-N (paenipeptin C) 2-4 [39]

Paenibacillus larvae ATCC 9545 Bacillus pumilus DSVP18 30-35 [21]

Yersinia enterocolitica* Paenibacillus sp. OSY-N (paenipeptin C) 0,5-1 [39]

Note: * — strain number not provided.

Table 3. Effect of rhamnolipids produced by the Arctic Sea bacteria on strains of Burkholderia

Test culture Inhibition of test cultures (%) in the presence of rhamnolipids, produced by

Pseudomonas BTN 1 Psychro-bacter BTN2 Psychro-bacter BTN15 Psychro-bacter BTN5 Arthro-bacter BTN 4

Burkholderia diffusa LMG 24065 100 75 77 77 63

Burkholderia metallica LMG 24068 92 70 71 77 64

Burkholderia cenocepacia LMG 16656 100 78 87 84 57

Burkholderia latens LMG 24064 100 53 75 58 41

Burkholderia seminalis LMG 24067 100 43 67 40 56

E264 (ATCC 700388) on glycerol, on their antimicrobial activity was studied in [63]. Chemical analysis of the rhamnolipids showed that strain E264 synthesizes the mixture of dirhamnolipids and monorhamnolipids in the ratio 3:1. Further research showed that dirhamnolipids have higher antimicrobial effect than monorhamnolipids. Meanwhile the highest antimicrobial activity was found in supernatant with unpurified rhamnolipid mixture which might be explained by synergy of the fractions or the presence of other compounds besides rhamnolipids with antimicrobial effect.

Aleksic et al. [64] studied antimicrobial activity of both the complex of rhamnolipids produced by Lysinibacillus sp. BV152.1 and its separate fractions. It was found that all

fractions of strain BV152.1 rhamnolipids had the same weak antimicrobial effect against P. aeruginosa PAO1, P. aeruginosa DM50, S. aureus ATCC 25923, S. aureus MRSA and S. marcescens ATCC 27117. Their MIC against all test cultures were 500 pg/ml.

The report [65] describes the isolation of a strain identified as P. aeruginosa LCD 12 which synthesizes the complex of mono-and dirhamnolipids, from samples of raw petroleum. The authors studied antimicrobial activity of the surfactant complex and of its constituents. It was found that MIC of all studied rhamnolipids against Streptococcus epidermidis, B. subtilis, S. aureus and E. coli were close: 4; 4; 16 and 4 pg/ml, respectively.

The data on rhamnolipid antimicrobial activity are summarized in Table 4.

Table 4. Minimum inhibitory concentrations of rhamnolipids

Test culture Producer MIC, ^g/ml References

Staphylococcus aureus 6538P Pseudomonas BTN 1 1.56-3.12 [61]

Staphylococcus aureus Pseudomonas aeruginosa LCD12 16 [65]

Staphylococcus aureus ATCC 25923 Lysinibacillus sp. BV152.1 500 [64]

Staphylococcus aureus* (methicillin-resistant) Lysinibacillus sp. BV152.1 500 [64]

Staphylococcus aureus ATCC 25923 Pseudomonas aeruginosa C2 650 [66]

Staphylococcus aureus ATCC 43300 (methicil-lin-resistant) Pseudomonas aeruginosa W10 9 370 [62]

Staphylococcus capitis SH6 Pseudomonas aeruginosa W10 18 750 [62]

Pseudomonas aeruginosa PAO1 Lysinibacillus sp. BV152.1 500 [64]

Pseudomonas aeruginosa DM50 Lysinibacillus sp. BV152.1 500 [64]

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Bacillus subtilis Pseudomonas aeruginosa LCD12 4 [65]

Bacillus licheniformis CAN55 Pseudomonas aeruginosa W10 1500 [62]

Escherichia coli Pseudomonas aeruginosa LCD12 4 [65]

Escherichia coli K8813 Pseudomonas aeruginosa C2 550 [66]

Esherchia coli ATCC 25922 Pseudomonas aeruginosa W10 37 500 [62]

Streptococcus epidermidis Pseudomonas aeruginosa LCD12 4 [65]

Streptococcus oralis Burkholderia thailandensis E264 150 [63]

Streptococcus sanguinis Burkholderia thailandensis E264 150 [63]

Neisseria mucosa Burkholderia thailandensis E264 150 [63]

Actinomyces naeslundii Burkholderia thailandensis E264 300 [63]

Serratia marcescens ATCC 27117 Lysinibacillus sp. BV152.1 500 [64]

Candida albicans ATCC 10231 Pseudomonas aeruginosa W10 2 340 [62]

Data in Table 5 show that the antibacterial activity of rhamnolipids as well as lipopeptides (Table 2) depends on the test culture (both species and strain) and on the complex of surfactants. Lipopeptides are more efficient antibacterial agents compared to rhamnolipids (Tables 2 and 5).

In a number of recent studies, the antibacterial activity of rhamnolipids was determined by the agar diffusion technique but not the MIC [22, 67-69]. Thus, supernatant (15 pl, with rhamnolipid concentration 0.57 g/l) obtained by culturing P. aeruginosa P1R16 on olive oil, the growth inhibition zones were the following: 11 mm for E. coli ATCC 25922, 25 mm for P. aeruginosa ATCC 27853, 12 mm for S. aureus ATCC 25923 and B. cereus CCT0198, and 22 mm for Ralstonia solanacearum 1226 [67].

In the presence 1.12 mg/ml rhamnolipids of P. aeruginosa SARCC 697 the diameters of growth inhibition zones for bacterial test cultures were (mm): 13.5 for E. coli ATCC 417373; 29.3 for E. coli ATCC 13706; 13.5 for Klebsiella pneumoniae ATCC 10031; 8.3 for K. pneumoniae P3; 20.3 for Salmonella typhimurium ATCC 14028; 14 for Salmonella enterica SE 19; 14 for Serratia marcescens ATCC 13880; 13.7 for S. aureus ATCC 25923; and 11.5 for S. aureus C2 [22]. Growth inhibition zone for methicillin-resistant strain S. aureus ATCC 43300 under the effect of rhamnolipids produced by P. aeruginosa 47T2 on the mixture of waste sunflower and olive oil was 10 mm [68].

Oluwaseun et al. [69] compared the antimicrobial activity of rhamnolipids of P. aeruginosa C1501 and Tween 80. The

Table 5. Action of surface-active substances synthesized by A. calcoaceticus IMV B-7241, N. vaccinii IMV B-7405 and R. erythropolis Ac-50l7 on some microorganisms

Strain Carbon source in the culture medium Minimum inhibitory concentration (^g/ml) against

Bacillus subtilis BT-2 Enterobacter cloaceae C-8 Staphylococcus aureus BMS-1 Proteus vulgaris PA-12 Escherichia coli IEM-1 Candida albicans D-6

A. calcoaceticus IMV B-7241 Ethanol 14 56 14 14 28 N.d.

Purified glycerol 4 2 4 N.d. 2 2

Waste of biodiesel production 16 4 8 N.d. 4 16

Refined sunflower oil 50 25 14 1.8 0.9 25

Waste sunflower oil 20 20 2.5 2.5 1.3 40

N. vaccinii IMV B-7405 Purified glycerol 45 180 90 90 45 45

Waste of biodiesel production 15 120 15 60 30 30

Refined sunflower oil 20 160 80 80 10 40

Waste sunflower oil 18 140 70 70 9 35

R. erythropolis IMV Ac-5017 Ethanol 60 240 N.d. N.d. 15 >480

Purified glycerol 15.6 N.d. 62.5 62.5 250 N.d.

Waste of biodiesel production 62.5 N.d. 125 31 125 N.d.

Note. N.d. — not determined

research showed that surfactants of strain C1501 were more effective antimicrobial agents compared to the chemical analogue. Thus, growth inhibition zones for S. aureus, B. cereus and E. coli with addition of 3 % rhamnolipid solution were 20-22 mm, and that of Tween at similar concentrations was only 5 mm.

Rhamnolipids action on fungi. Our paper [28] provides information on the antifungal activity of rhamnolipids aimed to manage the spread of phytopathogenic fungi, so our current review shall focus on further work.

Yan et al. [70] studied the effect of rhamnolipids of P. aeruginosa ZJU-211 on the phytopathogenic fungus Alternaria alternata. They found that at 125 pg/ml surfactant, growth of the fungus was inhibited only by 26.6%, and at 250 pg/ml rhamnolipids, by 40%. Raising the rhamnolipids concentration to 400-1000 pg/ml was followed by inhibition of the pathogenic spore germination by 64-81.7%. Treating tomatoes, infected with

A. alternata, with the mixture of rhamnolipids (500 pg/ml) and laurel oil (500 pg/ml) decreased the degree of infection to 43 %.

At 200 pg/ml, the surfactant complex and fractions of mono- and dirhamnoliipds of P. aeruginosa KVD-HM52 inhibited the growth of F. oxysporum NCIM1072 by 95 and 84%, respectively [71]. MIC of purified rhamnolipids against the micromycete was only 50 pg/ml.

Another study [72] considered the antifungal activity of rhamnolipids produced by P. aeruginosa No. 112 against Aspergillus niger MUM 92.13 and Aspergillus carbonarius MUM 05.18. It was established that the dirhamnolipids were responsible for the antifungal activity, while monorhamnolipids demonstrated weak inhibiting action. Besides that, the authors showed that adding NaCl to purified mono- and dirhamnolipids increased their antifungal effect. Thus, the mixture of dirhamnolipids of 0.375 g/l and 875 mM

NaCl fully inhibited growth of test cultures of A. niger MUM 92.13, while pure dirhamnolipid solution did it only by 40 %. Adding salt at the same concentration to monorhamnolipid solution was followed by inhibition of test culture only by 40 %, and monorhamnolipids without salt did not inhibit the fungal growth at all. The effect of added salt was explained by NaCl repairing structure of rhamnolipids which was disrupted in extraction from the culture medium.

Thus, research of antimicrobial activity of rhamnolipids is still fruitful. Though rhamnolipids are less efficient than lipopeptides in their antimicrobial action, they have a number of some advantages: firstly, the higher productivity of producers, and secondly, the possibility of synthesis on industrial waste, which decreased their cost.

Sophorolipid effect on microorganisms

Main producers of sophorolipids are yeasts of the genera Candida (Starmerella), Rhodotorula, and Wickerhamomyces [73]. A sophorolipid has a hydrophobic part (fatty acid) and a hydrophilic one (sophorose disaccharide with a P-1,2 bond), and sophorose can be acetylated on the 6' and/or 6'' position. The carboxyl group of the fatty acid can be free forming acid (non-lactone) structure or etherified on the 4'' position forming the lactone variant [73].

Most recent publications focused on the antimicrobial effect of sophorolipids produced by Candida (Starmerella) bombicola ATCC 22214 [74-79]. Thus, the authors of [74] studied antimicrobial properties of the glycolipids produced on glucose and lauryl alcohol (10%, v/v). They showed that the yeast culture on the lauryl alcohol produced lactone sophorolipids, which unlike surfactants obtained on glucose fully inhibited the growth of Gram-negative (E. coli ATCC 8739, P. aeruginosa ATCC 9027) and Gram-positive (S. aureus ATCC 6358, B. subtilis ATCC 6633) bacteria and of the yeast C. albicans ATCC 20910, at concentration 5-10 pg/ml. The data showed that the hydrophobic substrates are more suitable for production of sophorolipids with high antimicrobial activity.

Zhang et al. [75] analysed the antimicrobial activity of sophorolipids produced by C. bombicola ATCC 22214 on glucose with added palmitic, stearic and oleic acids as precursors. Irrespectively of the culture conditions, sophorolipids almost did not vary in antimicrobial activity against Salmonella spp. and Listeria spp.

In the paper [76] it was established that sophorolipids produced by C. bombicola ATCC 22214 on coconut oil had higher antimicrobial activity against E. coli and S. aureus, than if produced on corn oil. Quite probably the different antimicrobial activity of sophorolipids is caused by different length of acyl chain, yet the authors did not stress it.

Elshikh et al. [77] studied the effect of sophorolipids of C. bombicola ATCC 2221, on the oral pathogens. MIC of the sophorolipids against Streptococcus mutans DSM-20523, Streptococcus oralis DSM-20627; Actinomyces naeslundii DSM-43013, Neisseria mucosa DSM-4631 and Streptococcus sanguinis NCTC 7863 were 195, 97.5, 195, 97.5 and 195 pg/ml, respectively.

Solaiman et al. [78] studied the effect of culture condition of S. bombicola ATCC 22214 on its sophorolipid antimicrobial action on microbes destroying salt hides. They cultured the microbial source on medium with glucose (10 g/l) with co-substrate (2 g/l) of palmitic, stearic and oleic acids (the sophorolipids were referred to as SL-p, SL-s, SL-o). The experiments showed that MIC of SL-p and SL-o against Gram-positive (B. licheniformis, B. pumilus, Bacillus mycoides, Enterococcus faecium, Aerococcus viridans, Staphylococcus xylosus, Staphylococcus cohnii) and Gram-negative (Pseudomonas luteola, Enterobacter cloacae, Enterobacter sakazakii and Vibrio fluvialis) bacteria were the same (19.5 pg/ml), and MIC of SL-s were lower (4.88-9.76 pg/ml).

Later [79] the same authors studied antimicrobial action of sophorolipids of S. bombicola ATCC 22214 on bacteria of the genera Lactobacillus and Streptococcus, which cause dental caries. The growth of Lactobacillus acidophilus ATCC 4356 and Lactobacillus fermentum ATCC9338 was fully inhibited at 1.3 and 1.0 mg/ml sophorolipids, respectively. Meanwhile the MIC of the studied compounds against Streptococcus mutans ATCC 25175, Streptococcus salivarius ATCC 13419 and Streptococcus sobrinus ATCC 33478 were only 20-38 pg/ml.

In 2017, sophorolipids produced by Rhodotorula babjevae YS3 on a medium with glucose (10 g/l) were shown to have antifungal effect [80]. MIC against Colletotrichum gloeosporioides was 62 pg/ml. Comparatively, MIC against Fusarium verticilliodes, Fusarium oxysporum f. sp. pisi was 125 pg/ml, while that against Corynespora cassiicola and

Table 6. Advantages and disadvantages of different microbial surfactants as antimicrobial agents

Surfactant Advantages Disadvantages

Rhamnolipids Possible synthesis on industrial waste; high surfactant content Producers belong to conditionally pathogenic microorganisms; antimicrobial activity not high enough

Lipopeptides Low minimum inhibiting concentrations against a wide range of pathogenic microorganisms Low content of produced surfactants; narrow range of substrates for surfactant synthesis (mostly carbohydrates); antimicrobial activity depends on culture conditions

Sophorolipids Synthesis on cheap substrates (waste oil, oil production waste); High antimicrobial activity at low surfactant concentrations Low product yield relative to substrate; sources belong to conditionally pathogenic microorganisms; antimicrobial activity depends on culture conditions

Complex of amino- and glycolipids of strains IMV В-7241, IMV В-7405 and IMV Ас-5017 Synthesis on waste (waste oil, waste of biodiesel production); High antimicrobial activity at low surfactant content Antimicrobial activity depends on the culture conditions

Trichophyton rubrum was much higher (2000 and 1000 pg/ml, respectively).

Therefore, the antimicrobial activity of sophorolipids is higher than that of rhamnolipids. Sophorolipids have a wide range of antimicrobial action on Gramnegative and Gram-positive bacteria and fungi. Publications of the recent years seldom show that sophorolipid antimicrobial activity depends on the culture conditions, such as the carbon source and the presence of precursors for biosynthesis.

Antimicrobial activity of Acinetobacter calcoaceticus IMV В-7241, Rhodococcus erythropolis IMV Ac-5017 and Nocardia vaccinii IMVВ-7405 surfactants

We have already established [81] that chemically the surfactants of R. erythropolis IMV Ac-5017 are a complex of glyco-(trehalose mono- and dimycolate), neutral (cetyl alcohol, palmitic acid, methyl ester of n-pentadecane acid, mycolic acids) and phospholipids (phosphatidylglycerol, phosphotidylethanolamine). Glyco- and aminolipids were found in the surfactant of A. calcoaceticus IMV В-7241, and N. vaccinii IMV В-7405 produces a complex of neutral, glyco- and aminolipids [81].

Table 5 presents the MIC of surface-active substances produced by strains IMV Ac-5017, IMV В-7241 and IMV В-7405 on various carbon substrates against bacteria and yeasts. The data show that the antimicrobial activity

of A. calcoaceticus IMV B-7241, N. vaccinii IMV B-7405 and R. erythropolis IMV Ac-5017 surfactants depends on the culture conditions, which agrees with data obtained by other researchers in the recent reports [25, 34, 74, 76, 78]. Notably, the surfactants we studied had no higher MIC then described elsewhere.

* * *

We analysed the recent literature on the antimicrobial properties of suface-active substances produced by different groups of microorganisms as an alternative for antibiotics, chemical biocides and desinfectants. The as-yet few papers and our own results do support the necessity of studying the influence of culture conditions on antimicrobial activity of the synthesized surfactants.

The well-known microbial surfactants are compared in Table 6. It shows that the microbial surfactants have their advantages and disadvantages. A strong advantage is the possibility for culturing on industrial waste, which not only lowers the production cost but helps utilize waste of other industries.

The dependency of the substances' antimicrobial activity on the culture conditions can be regulated by chemical modification [82, 83], by genetically [58, 84, 85] and methabolically [86, 87] engineering strains, and by implementing physiological approaches described in [88-90].

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АНТИМ1КРОБНА АКТИВН1СТЬ ПОВЕРХНЕВО-АКТИВНИХ РЕЧОВИН М1КРОБНОГО ПОХОДЖЕННЯ

Т. П. Пирог Д. А. Луцай Л. В. Ключка Х. А. Берегова

Нащональний ушверситет харчових технологш, Кшв

E-mail: tapirog@nuft.edu.ua

Метою роботи було проаналiзувати лггера-туру останшх рокiв щодо антибактерiальноï та антифунгальноï активнiстi мiкробних поверх-нево-активних речовин (ПАР) (лiпопептидiв, синтезованих представниками родiв Bacillus, Paenibacillus, Pseudomonas, Brevibacillus, рамнолiпiдiв бактерiй родiв Pseudomonas, Burkholderia, Lysinibacillus, софоролшь дiв дрiжджiв родiв Candida (Starmerella та Rhodotorula), а також данi власних експери-ментальних дослiджень антимiкробноï активной ПАР, синтезованих Acinetobacter calcoaceticus 1MB В-7241, Rhodococcus erythropolis 1MB A^5017 i Nocardia vaccinii 1MB B-7405. Проведений аналiз показав, що ль попептиди e ефективнiшими антимшробними агентами порiвняно з глiколiпiдами. Мшмаль-нi iнгiбувальнi концентрацiï (М1К) лшопепти-дiв, рамнолiпiдiв i софоролiпiдiв становлять у середньому (мкг/мл): 1-32, 50-500 i 10-200 вщповщно. М1К поверхнево-активних речовин, синтезованих штамами 1MB В-7241, 1MB Ас-5017 i 1MB B-7405, — у межах, визначених для вщомих лiпопептидiв та глiколiпiдiв. Перевагами глшолшЩв як антимiкробних аген-тiв порiвняно з лiпопептидами e можлив^ть ïx синтезу на промислових вщходах i висока кон-центращя синтезованих ПАР. Нечисленнi даш лггератури i власнi результати авторiв свщчать про необхiднiсть проведення дослiджень щодо впливу умов культивування на антимшробну актившсть цiльового продукту.

Ключовi слова: мшробш лiпопептиди, рамно-лiпiди та софоролшщи, антибактерiальна та антифунгальна актившсть.

АНТИМИКРОБНАЯ АКТИВНОСТЬ ПОВЕРХНОСТНО-АКТИВНЫХ ВЕЩЕСТВ МИКРОБНОГО ПРОИСХОЖДЕНИЯ

Т. П. Пирог Д. А. Луцай, Л. В. Ключка К. А. Береговая

Национальный университет пищевых технологий, Киев, Украина

E-mail: tapirog@nuft.edu.ua

Целью работы был анализ данных литературы последних лет относительно антибактериальной и антифунгальной активности микробных поверхностно-активных веществ ^AB) (липопептидов, синтезированных представителями родов Bacillus, Paenibacillus, Pseudomonas, Brevibacillus, рамнолипидов бактерий родов Pseudomonas, Burkholderia, Lysinibacillus, софоролипидов дрожжей родов Candida (Starmerella и Rhodotorula), а также собственных экспериментальных исследований антимикробной активности ПAB, синтезированных Acinetobacter calcoaceticus 1MB B-7241, Rhodococcus erythropolis 1MB Aс-5017 и Nocardia vaccinii 1MB B-7405. Проведенный анализ показал, что липопептиды являются более эффективными антимикробными агентами по сравнению с гликолипидами. Mини-мальные ингибирующие концентрации ^ИК) липопептидов, рамнолипидов и софоролипидов составляют в среднем (мкг/мл): 1-32, 50-500 и 10-200 соответственно. MИК поверхностно-активных веществ, синтезированных штаммами IMB B-7241, 1MB Ас-5017 и 1MB B-7405, находятся в пределах, установленных для известных липопептидов и гликолипидов. Преимуществами гликолипидов как антимикробных агентов по сравнению с липопептидами являются возможность их синтеза на промышленных отходах и высокая концентрация синтезированных ПAB. Немногочисленные данные литературы и собственные результаты авторов свидетельствуют о необходимости проведения исследований влияния условий культивирования продуцентов на антимикробную активность целевого продукта.

Ключевые слова: микробные липопептиды, рамнолипиды и софоролипиды, антибактериальная и антифунгальная активность.

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