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Review

Marine Aspergillus: A Treasure Trove of Antimicrobial Compounds

by
Honghua Li
,
Yanqi Fu
and
Fuhang Song
*
Key Laboratory of Geriatric Nutrition and Health, Ministry of Education of China, School of Light Industry, Beijing Technology and Business University, Beijing 100048, China
*
Author to whom correspondence should be addressed.
Mar. Drugs 2023, 21(5), 277; https://doi.org/10.3390/md21050277
Submission received: 31 March 2023 / Revised: 22 April 2023 / Accepted: 25 April 2023 / Published: 28 April 2023
(This article belongs to the Special Issue Diversity of Marine Fungi as a Source of Bioactive Natural Products)
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Abstract

:
Secondary metabolites from marine organisms are diverse in structure and function. Marine Aspergillus is an important source of bioactive natural products. We reviewed the structures and antimicrobial activities of compounds isolated from different marine Aspergillus over the past two years (January 2021–March 2023). Ninety-eight compounds derived from Aspergillus species were described. The chemical diversity and antimicrobial activities of these metabolites will provide a large number of promising lead compounds for the development of antimicrobial agents.

1. Introduction

Compared with terrestrial fungi, marine fungi are more abundant in species. Due to the complex environment, their metabolites have novel structures and diverse activities [1,2,3,4]. As an important member of marine microorganisms, fungi play an important role in the study of active natural products. Marine fungi can be obtained from marine animals, plants, sediments and seawater [5,6,7,8]. Therefore, marine fungi have a wide range of sources [6,9,10,11,12,13,14,15].
Aspergillus is a genus of fungi widely distributed in marine environments [16,17,18]. Common species include A. fumigatus, A. niger, A. versicolor, A. flavus, A. ochraceu, A. ticus, A. terreus, etc. Marine Aspergillus is an important resource in the production of active natural products, such as steroids, flavonoids, azolones, etc. [7,19,20,21,22]. These metabolites are structurally diverse and exhibit a wide range of biological activities, including anticancer, antiviral, antibacterial, anti-inflammatory, lipid-lowering and anti-diabetic [22,23,24,25,26,27].
Due to the wide range of Aspergillus sources, the diverse secondary metabolites and the wide biological activities, the research on Aspergillus metabolites has attracted much attention. Therefore, a series of excellent reviews on this subject have been published so far [28,29,30,31,32,33,34,35,36,37,38,39]. In 2016, Fouillaud et al. reviewed the knowledge of anthraquinones and their derivatives derived from filamentous fungi [40]. In 2022, Hafez Ghoran et al. updated this study and summarized and classified the structures and activities of 296 anthraquinones and their derivatives [41]. In 2019, Youssef et al. reviewed the chemical and biological activities of peptides which isolated and identified from marine fungi [22]. 131 peptides were reported from these 17 genera, and about 53% of the isolated peptides showed cytotoxic, antibacterial and antiviral activities. In 2020, Jiang et al. reviewed the chemical structure and bioactive properties of new terpenes from marine derived fungi, as well as the biodiversity of these fungi from 2015 to 2019 [19]. Penicillium, Aspergillus and Trichoderma fungi were the main producers of terpenes. In 2021, Rani et al. reviewed the research status of microbial antibacterial molecules [10]. In 2022, Li et al., reviewed the chemistry and bioactivity of marine-derived bisabolane sesquiterpenoids [1]. In 2013, Lee et al. reviewed the bioactive secondary metabolites of Aspergillus derived from marine sources [42]. In 2018, Wang et al. reviewed 232 new bioactive metabolites from Aspergillus of marine origin from 2006 to 2016 and classified their bioactivity and chemical structures [43]. In 2020, Xu et al. reviewed the structural diversity and biological activity of 130 heterocyclic alkaloids produced by Aspergillus of marine origin from early 2014 to late 2018 [44]. However, there have been no studies on the antimicrobial compounds from marine Aspergillus in the last two years despite the fact that over the past two years, reports of antibacterial metabolites from Aspergillus have increased [45,46,47,48,49,50,51]. It is believed that the study of Aspergillus living in marine environments will facilitate the isolation of new fungal species and lead to the discovery of new compounds. Therefore, this review updates current compounds to cover metabolites isolated from marine Aspergillus between January 2021 and March 2023. It also provides structural diversity of compounds, as well as detailed information on sources and associated antimicrobial activity. We introduced the structural diversity and antimicrobial activity of 98 compounds isolated from marine-derived Aspergillus. This study will contribute to a better understanding of the chemical properties and biological activities of natural products from marine Aspergillus, thus facilitating drug discovery and development.

2. Aspergillus sp. from Various Marine Sources and Their Antimicrobial Activities

2.1. Aspergillus sp. from Marine Animals and Their Antimicrobial Activities

Trypacidin (1) was isolated from the A. fumigatus HX-1 associated with clams (Figure 1). The anti-Vibrio harveyi activity of trypacidin was the same as that of streptomycin sulfate, and the minimum inhibitory concentration (MIC) was 31.25 μg/mL [52].
Two new dipeptides, asperopiperazines A and B (2 and 3), were obtained from Aspergillus sp. DY001 (Figure 1). The MICs of asperopiperazines A and B against Escherichia coli were 8 and 4 μM, and 8 and 8 μM against S. aureus, respectively [53].
In conclusion, only two Aspergillus species producing antimicrobial compounds are found from marine animals (except sponges and corals). Three compounds from these two Aspergillus strains have been reviewed for their antimicrobial activities. Notably, asperopiperazines A and B from Aspergillus sp. DY001 showed potent antimicrobial activities against E. coli and S. aureus.

2.2. Aspergillus sp. from Marine Plants and Their Antimicrobial Activities

Six new terpenoids were isolated from a seaward fungus A. alabamensis (Figure 2). They are asperalacids A-E and 4-hydroxy-5-(6)-dihydroterrecyclic acid A (4). Compound 4 and asperalacids A–D (5–8) showed antimicrobial activities against plant pathogenic fungi Penicillium italicum, Fusarium graminearum and F. oxysporum, as well as S. aureus and the Gram-positive bacteria Bacillus subtilis. Both MICs of asperalacids A and D against F. graminearum were 200 μg/mL. The MIC of asperalacids B and C against F. oxysporum were 100 and 100 μg/mL, and 200 and 25 μg/mL against F. graminearum, respectively. The MIC of compound 8 against P. italicum, F. graminearum, F. oxysporum and S. aureus were 200, 50, 100 and 25 μg/mL, respectively [54].
Eight new benzoic acid-containing alkaloids were isolated and identified from A. alabamensis. Among these compounds, asperalins A–F (9–14) showed moderate or strong inhibitory activities against some fish pathogens, Streptococcus parauberis, S. iniae and Edwardsiella ictalurid (Figure 2). Asperalins C and D showed strong antibacterial activities against S. aureus, S. parauberis and S. iniae, with MIC values of 10.1, 10.1 and 5.0 μM, respectively. Asperalin E had the strongest inhibitory effect on S. iniae with an MIC value of 2.2 μM. Notably, the MICs of asperalin F against four Gram-positive bacteria S. aureus, B. subtilis, S. parauberis, S. iniae and one Gram-negative bacterium E. ictalurid were 21.8, 87.3, 21.8, 43.6 and 10.9 μM, respectively [55].
In conclusion, Aspergillus species and its active metabolites from marine plant sources (except mangrove and seagrasses) were summarized. Eleven antimicrobial compounds were identified in the seagrass-derived fungus A. alabamensis during 2022 and 2023. Compounds 4–8 had a weak inhibitory effect on plant pathogens. However, compounds 11–14 showed strong antibacterial effects against S. aureus, S. iniae and some Gram-positive bacteria.

2.3. Aspergillus sp. from Mangroves and Their Antimicrobial Activities

Six antibacterial compounds were isolated from the marine fungus A. brunneoviolaceus MF180246 (Figure 3). These compounds included asperbrunneo acid (15), secalonic acid H (16), chrysoxanthone C (17), secalonic acid F1 (18), asperdichrome (19) and penicillixanthone A (20). They showed antibacterial activity against S. aureus with MIC values of 200, 50, 50, 25, 25 and 6.25 μg/mL [27].
Six polyhydroxy p-terphenyls (asperterphenyllins A–F) were isolated from the endophytic fungus A. candidus LDJ-5 in mangroves. Only asperterphenyllin C (21) showed antibacterial activity against Proteus sp. with an MIC value of 19 μg/mL [56].
Two new heterodimeric tetrahydroxanthones, aflaxanthones A and B (22 and 23), were isolated from A. flavus QQYZ. These two compounds showed potential antimicrobial activity and broad spectrum against several pathogenic fungi such as C. albicans and F. oxysporum, with MIC values in the range of 3.13–50 μM. They also showed moderate antibacterial activity against several bacteria such as B. subtilis and methicillin-resistant S. aureus (MRSA), with MIC values in the range of 12.5–25 μM [57].
In conclusion, Aspergillus and its active metabolites from mangroves were summarized. Due to the special geographical environment, mangroves had a wide variety of organisms, which has been thoroughly examined in previous studies of metabolites. Nine antimicrobial compounds were found in three Aspergillus strains from mangrove sources. Most of the compounds showed moderate antimicrobial activities. Among these compounds, compound 20 showed a strong inhibitory effect on S. aureus.

2.4. Aspergillus sp. Derived from Algae and Their Antimicrobial Activities

Two C7-alkylated salicylaldehyde derivatives metabolites, namely asperglaucins A and B (24 and 25), were isolated from the endophytic fungus A. chevalieri SQ-8 (Figure 4). Asperglaucins A and B showed potent antimicrobial activities against plant pathogens B. cereus and Pseudomonas syringae pv actinidae (Psa), with an MIC value of 6.25 μM. Further analysis showed that asperglaucins A and B may change the external structure of B. cereus and Psa and cause cell membrane rupture or deformation. The results indicated that asperglaucins A and B may be potential lead compounds of pesticide fungicides [58].
Two new diketopiperazines, namely versiamide A (26) and 3, 15-dehydroprotuboxepin K (27), were isolated from endophytic fungus A. creber EN-602 obtained from the marine red algae Rhodomela confervoides. Versiamide A and 3, 15-dehydroprotuboxepin K showed inhibitory activities against a variety of aquatic bacteria, with MIC values ranging from 8 to 64 μg/mL. Versiamide A showed antibacterial activity against Aeromonas hydrophila, E. coli, Micrococcus luteus and P. aeruginosa, with MIC values of 64, 16, 64 and 64 μg/mL. 3, 15-dehydroprotuboxepin K showed antibacterial activity against E. tarda, E. coli, M. luteus, P. aeruginosa and V. harveyi, with MIC values of 64, 8, 16, 32 and 64 μg/mL [59].
An antibacterial terpenoid, namely terretonin F (28), were isolated from the Aspergillus sp. RR-YLW12, which derived from marine red algae R. confervoide. Terretonin F showed significant inhibitory activities against Chattonella marina, Heterosigma akashiwo and Prorocentrum donghaiense, with IC50 values of 3.1, 5.2 and 10.5 μg/mL, respectively [60].
In conclusion, Aspergillus species from marine algae and active metabolites were summarized. Five antimicrobial compounds were found in three fungi strains of algae origin. It should be noted that asperglaucins A and B (24 and 25) showed a strong inhibitory effect on B. cereus. The possible bacteriostatic mechanism of the compounds was also introduced. At present, the studies on the structure and biological activity of compounds are abundant, but the studies on the mechanism of biological activity are limited.

2.5. Aspergillus sp. from Corals and Their Antimicrobial Activities

Three known metabolites, including demethylincisterol A2 (29), asperophiobolin E (30) and butyrolactone I (31), were isolated and identified from the soft coral fungus A. hiratsukae SCSIO 5Bn1003 (Figure 5). Compounds 29–31 showed potent antibacterial activity against B. subtilis, with MIC values of 10.26 ± 0.76, 17.00 ± 1.25 and 5.30 ± 0.29 μM. Meanwhile, asperophiobolin E and butyrolactone I showed weak activity against S. aureus, with MIC values of 102.86 ± 4.50 and 59.54 ± 0.50 μM, respectively [61].
Five new antimicrobial α-pyranone methterpenoids H-L (32–36) and one known antimicrobial compound, namely neoechinulin A (37), were isolated from A. hiratsukae SCSIO 7S2001, a fungus derived from ophiophora coral. Methterpenoids H-L and neoechinulin A showed varying degrees of antibacterial activity, with MIC values of 6.25–100 μg/mL. The MIC values of methterpenoid H were 6.25 μg/mL for Micrococcus lutea 01, MRSA, and Streptococcus faecalis; that of methterpenoid I was 6.25 μg/mL for MRSA; that of methterpenoid G was 12.5 μg/mL for MRSA; that of methterpenoid K was 6.25 μg/mL for Klebsiella pneumoniae; that of methterpenoid L was 12.5 μg/mL for M. lutea, S. faecalis and MRSA; and that of neoechinulin A was 12.5 μg/mL for S. faecalis. [62].
Two butenolides, including versicolactone B (38) and butyrolactone VI (39), were isolated from Aspergillus terreus SCSIO41404, a fungus derived from coral. Versicolactone B and butyrolactone VI showed weak antibacterial activity against Enterococcus faecalis and K. pneumoniae with IC50 values of 25 and 50 μg/mL, respectively [63].
Six chlorinated polyketones were isolated from the coral fungus A. unguis GXIMD 02505 in the Beibu Gulf. These polyketones included aspergillusethers J and F (40 and 41), nornidulin (42), aspergillusidones B and C (43 and 44) and 1-(2, 6-dihydroxy-4-methoxy-3, 5-dimethylphenyl)- 2-methylbutan-1-one (45). Compounds 40–45 exhibited inhibitory activities against marine biofilm-forming bacteria, Marinobacterium jannaschii, MRSA, Microbulbifer variabilis and Vibrio pelagius, with MIC values ranging from 2 to 64 μg/mL [64].
Five antimicrobial cyclic lipopeptides, namely maribasins C-E (46–48) and maribasins A and B (49 and 50), were isolated from the marine fungus Aspergillus sp. SCSIO 41501. These compounds showed strong antifungal activities against five plant pathogenic fungi, with MIC values ranging from 3.12 to 50 μg/disc [34].
In conclusion, coral-derived Aspergillus and its active metabolites were summarized. Twenty-two antimicrobial compounds were found in five fungi strains of coral origin. It was a relatively large variety of compounds compared with Aspergillus from other origins. Most of the compounds had a wide antimicrobial spectrum against different bacteria and fungi.

2.6. Aspergillus sp. Derived from Sponges and Their Antimicrobial Activities

One hydroxypyrrolidine alkaloid preussin (51) was isolated and identified from marine sponge-related fungus A. candius KUFA 0062 (Figure 6). Preussin showed inhibition against vancomycin-resistant Enterococcus (VRE) and MRSA, as well as E. faecalis ATCC29212 and S. aureus ATCC 29213 [65].
Four antimicrobial compounds were isolated from the marine sponge-derived fungus Aspergillu flavus KUFA1152. These compounds were aspulvinones B’, H, R and S (52–55). Aspulvinones B’, H, R and S showed antibacterial activity against some multidrug-resistant strains isolated from the environment, and inhibited the biofilm formation of strains. Aspulvinones B’ and H displayed activity with MIC values of 16 μg/mL for the S. aureus, and for E. faecalis, MIC values ranged from 16 to 64 μg/mL. Aspulvinones R and S exhibited the potent activity against all Gram-positive strains tested, with MIC values ranging from 4 to 16 μg/mL for S. aureus and E. faecalis, and from 8 to 16 μg/mL for the VRE and MRSA [66].
The endophytic fungus A. niger L14 has been chemically studied, and two dimers, naphtho-γ-pyrone, fonsecinone A (56) and isoaurasperone A (57), have been isolated. These compounds had obvious inhibitory effects on human pathogenic bacteria Helicobacter pylori 159 and G27 with MIC values ≤ 4 μg/mL, comparable to the antibacterial effect of ampicillin sodium [67].
One antimicrobial compound, namely dizinc hydroxy-neotriamycin (58), was isolated from the sponge-related fungus A. ochraceopetaliformis SCSIO 41018. Dizinchydroxyneoaspergillin showed potent inhibition against MRSA, Acinetobacter baumannii, E. faecalis, Staphyloccocus aureus and Klebsiella pneumonia, with MIC values ranging from 0.45 to 7.8 μg/mL [68].
Two new chlorinated biphenyls, including aspergetherins A and C (59 and 60), and two known biphenyl derivatives, including methyl 3, 5-dichloroasterric acid (61) and methyl chloroasterrate (62), were isolated from a marine sponge symbiotic fungus A. terreus 164018. The antibacterial activity of these compounds against MRSA was evaluated, with MIC values ranging from 1.0 to 128 μg/mL. Notably, compound 61 had obvious inhibitory effects on two different MRSA strains, with MIC values of 1 and 16 μg/mL [69].
Chemical studies of the natural compounds of the marine fungus Aspergillus sp. LS57 had resulted in the isolation of aspergilluone A (63). The MIC value of aspergilluone A was 32 μg/mL against Mycobacterium tuberculosis, 64 μg/mL against S. aureus, and 128 μg/mL against both Gram-positive B. subtilis and Gram-negative E. coli [70].
Two novel tetracyclic skeleton alkaloids were isolated from Aspergillus sp. LS116, which were perinadines B and C (64 and 65). Perinadines B and C showed moderate antibacterial activity for B. subtilis with MIC values of 32 and 64 μg/mL [71].
In conclusion, Aspergillus and its active metabolites of sponge were summarized in this paper. Sponges are the most primitive marine animals with a large number of microorganisms, which are important sources of active natural products. Fifteen antibacterial compounds were found in seven fungi strains derived from sponge. Aspergillus derived from sponge was the source of antimicrobial compounds. Most of the compounds had a wide antimicrobial spectrum against a variety of bacteria and fungi. Hydroxy-neotriamycin (58) had a strong bacteriostatic effect on a variety of bacterial pathogens.

2.7. Aspergillus sp. from Seawater and Their Antimicrobial Activities

Nine antimicrobial compounds were isolated from marine fungus A. fumigatus H22. These compounds included 12,13-dihydroxyfumitremorgin C (66), fumitremorgin B (67), 13-oxofumitremorgin B (68), fumagillin (69), helvolic acid (70), 6-O-propionyl-16-O-deacetylhelvolic acid (71), 16-O-propionyl-6-O-deacetylhelvolic acid (72), penibenzophenone E (73) and sulochrin (74) (Figure 7). Compounds 66 and 68 showed potent antibacterial activity, and 69–74 exhibited strong anti-MRSA activity with MIC values between 1.25 and 2.5 μM. Additionally, compound 66 showed moderate inhibitory activity against Mycobacterium Bovis, with an MIC value of 25 μM, and compound 67 showed moderate inhibitory activity against C. albicans, with an MIC value of 50 μM [72].
Three novel phenolic polyketones, namely unguidepside C (75), aspersidone B (76) and agonodepside C (77), were isolated from A. unguis. These compounds showed a strong activity against Gram-positive bacteria, with MIC ranging from 5.3 to 22.1 μM [73].
Five novel dimeric tetrahydroxanthones, including aculeaxanthones A-E, were extracted from the marine fungus A. aculeatinus WHUF0198. Among them, only aculeaxanthone A (78) showed activity against B. subtilis 168, S. aureus USA300, H. pylori 159, H. pylori 129, H. pylori 26695 and H. pylori G27, with MIC values of 1.0, 2.0, 2.0, 2.0, 4.0 and 4.0 μg/mL, respectively [74].
In conclusion, Aspergillus and its active metabolites from seawater were summarized. Thirteen antimicrobial compounds were found in three fungi strains derived from seawater. Compounds 69–74 exhibited strong anti-MRSA activity and aculeaxanthone A (78) showed strong anti-bacterial pathogen activity.

2.8. Aspergillus sp. from Marine Sediments and Their Antimicrobial Activities

Six known compounds, including cyclopiamide (79), speradine H (80), speradine G (81), speradine B (82), speradine C (83) and cyclopiazonic acid (CPA) (84), were isolated from A. flavus SCSIO F025 from deep-sea sediments in the South China Sea (Figure 8). Compounds 79–84 showed weak antibacterial activity against E. coli, and CPA also exhibited strong antibacterial activity against MRSA, B. subtilis, S. aureus, M. luteus and Bacillus thuringiensis [75].
Five novel antibacterial metabolites and one known antibacterial compound were all isolated from the deep-sea sediment-derived fungus A. fumigatus SD-406. The novel metabolites included secofumitremorgins A and B (85a and 85b), 29-hydroxyfumiquinazoline C (86), 10R-15-methylpseurotin A (87), 1,4,23-trihydroxy-hopan-22,30-diol (88) and sphingofungin I (89), and one known cyclotryprostatin B (90). Compounds 85–90 exhibited inhibitory activities against pathogenic bacteria and plant pathogenic fungi, with MIC values of 4–64 μg/mL [76].
One new metabolite, namely 3, 5-dimethylorsellinic acid-based meroterpenoid (91), was isolated from the deep-sea fungus Aspergillus sp. CSYZ-1. Compound 91 showed strong antimicrobial activity against S. aureus and H. pylori, with MIC values of 2–16 and 1–4 μg/mL, respectively [77].
Two novel antibacterial metabolites, including aspergiloxathene A (92) and Δ2′-1′-dehydropenicillide (93) and one known antibacterial compound, namely dehydropenicillide (94), were isolated from Aspergillus sp. IMCASMF180035. Aspergiloxathene A exhibited significant inhibition against MRSA and S. aureus, with MIC values of 22.40 and 5.60 μM. Dehydropenicillide and Δ2′-1′-dehydropenicillide showed potent antibacterial activities against H. pylori, with MIC values of 21.61 and 21.73 μM, respectively [30].
One alkaloid asperthrin A (95) had been isolated from the marine endophytic fungus Aspergillus sp. YJ191021. The isolated compound had inhibitory effects on Rhizoctonia solani, Xanthomonas oryzae pv. Oryzicola and Vibrio anguillarum, with MIC values of 25, 12.5 and 8 μg/mL, respectively [78].
Three antimicrobial compounds were isolated from the fermented extracts of Aspergillus sp. WHUF05236. They included 6,8-di-O-methylversicolorin A (96), 6,8,1′-tri-O-methylaverantin (97) and 6,8-di-O-methylaverantin (98). They exhibited antibacterial activity against H. pylori, with MIC values ranging from 20.00 to 43.47 μM [79].
In conclusion, Aspergillus and its active metabolites from marine sediments were summarized. Twenty antimicrobial compounds were found in six Aspergillus strains from marine sediments. According to the literature, more than fifty antimicrobial compounds were produced by Aspergillus from marine sediments between 2018 and 2020. Therefore, marine sediments are an important source of secondary metabolites of fungi. Among them, compound 91 showed strong antimicrobial activity against S. aureus and H. pylori.
Sources and activities of compounds from marine Aspergillus were summarized in Table 1. We classified fungi and compounds according to Aspergillus origin.
In recent years, marine fungi have attracted the attention of researchers due to their bioactive compounds [10,44,46,80,81,82,83,84,85]. Combined with a series of previous excellent literature reviews, we conducted a comprehensive literature review of antibacterial compounds produced by Aspergillus fungi of different marine origin during the period of 2021–2023. The reported numbers of Aspergillus from marine animals, plants, mangroves, seagrasses, coral, sponge, seawater and marine sediment are shown in Figure 9. The most Aspergillus was derived from sponges, accounting for 23.30%. Aspergillus derived from marine coral was found in the second place, accounting for 16.7%.
We summarized ninety-eight antibacterial compounds from Aspergillus strains isolated from different marine sources (Figure 10). Among them, twenty-two antimicrobial compounds were found in marine corals from January 2021 to March 2023. Marine sediments had the next highest number of antimicrobial compounds, with twenty compounds. Therefore, in recent years, the antimicrobial compounds of Aspergillus from marine sources mainly came from marine corals and marine sediments. Marine natural products are rich in species and play an obvious role in the treatment of pathogen infections [86,87,88,89,90,91,92]. More and more novel compounds with different chemical structures and biological activities are being discovered [48,93,94,95,96,97,98,99].

3. Conclusions

This review describes antimicrobial compounds from Aspergillus species during January 2021 to March 2023. Ninety-eight compounds derived from Aspergillus species were described. Only three compounds with antimicrobial activities are found from marine animals (except sponges and corals). Twenty-two antimicrobial compounds were found in five fungi strains of coral origin. Fifteen antibacterial compounds were found in seven fungi strains derived from sponge. Most of these thirty-seven compounds had a wide antimicrobial spectrum against a variety of bacteria and fungi. Except for the compounds derived from coral and sponge, most of the compounds from other sources showed antibacterial activity, but no fungal inhibitory activity. Most of the compounds had inhibitory effects on S. aureus. Some compounds exhibited inhibitory effects on E. coli and B. subtilis. Among them, compound 91 showed strong antimicrobial activity against H. pylori. These active compounds have potential applications in bacterial and fungal infections and will provide reference for the development of novel anti-infective drugs.

Author Contributions

Writing—original draft preparation and editing, H.L.; writing—original draft preparation, Y.F.; writing—review and editing, H.L. and F.S.; supervision, F.S.; funding acquisition, H.L. and F.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by grants from the General Projects of Science and Technology Program of Beijing Municipal Education Commission (KM202210011008), Research Foundation for Young Teachers of Beijing Technology and Business University (QNJJ2022-21).

Data Availability Statement

Not applicable.

Acknowledgments

The authors gratefully acknowledge the financial supports.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Compounds of Aspergillus sp. derived from marine animals.
Figure 1. Compounds of Aspergillus sp. derived from marine animals.
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Figure 2. Compounds of Aspergillus sp. derived from marine plants.
Figure 2. Compounds of Aspergillus sp. derived from marine plants.
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Figure 3. Compounds of Aspergillus sp. derived from mangroves.
Figure 3. Compounds of Aspergillus sp. derived from mangroves.
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Figure 4. Compounds of Aspergillus sp. derived from algae.
Figure 4. Compounds of Aspergillus sp. derived from algae.
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Figure 5. Compounds of Aspergillus sp. derived from corals.
Figure 5. Compounds of Aspergillus sp. derived from corals.
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Figure 6. Compounds of Aspergillus sp. derived from sponges.
Figure 6. Compounds of Aspergillus sp. derived from sponges.
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Figure 7. Compounds of Aspergillus sp. derived from seawater.
Figure 7. Compounds of Aspergillus sp. derived from seawater.
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Figure 8. Compounds of Aspergillus sp. derived from marine sediments.
Figure 8. Compounds of Aspergillus sp. derived from marine sediments.
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Figure 9. The proportion of Aspergillus from different marine sources.
Figure 9. The proportion of Aspergillus from different marine sources.
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Figure 10. The proportion of Aspergillus compounds from different marine sources.
Figure 10. The proportion of Aspergillus compounds from different marine sources.
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Table
Table 1. Sources and activities of compounds from marine Aspergillus.
Table 1. Sources and activities of compounds from marine Aspergillus.
Sources and AspergillusCompoundsActivitiesReferences
Marine animals
A. fumigatus HX-1Trypacidin (1)MIC (anti-V. harveyi) was 31.25 μg/mL[52]
Aspergillus sp. DY001Asperopiperazines A, B (2, 3)MIC (anti-E. coli) were 8 and 4 μM MIC (anti-S. aureus) were 8 and 8 μM[53]
Marine plants
A. alabamensis4-hydroxy-5(6)-dihydroterrecyclic acid A (4),
asperalacids A–D (5–8)		MIC (anti-plant pathogens) was 25–200 μg/mL[54]
A. alabamensisasperalins A–F (9–14)MIC (anti-fish pathogens) was 2.2–87.3 μM[55]
Mangroves
A. brunneoviolaceus MF180246asperbrunneo acid (15),
secalonic acids H, F1 (16, 18), chrysoxanthone C (17), asperdichrome (19), penicillixanthone A (20)		MIC (anti-S. aureus) were 200, 50, 50, 25, 25, 6.25 μg/mL[27]
A. candius LDJ-5asperterphenyllin C (21)MIC (anti-Proteus sp.) was 19 μg/mL[56]
A. flavus QQYZaflatoxones A, B (22, 23)MIC (anti-pathogens) was 3.13–50 μM[57]
Marine algaes
A. chevalieri SQ-8asperglaucins A, B (24, 25)MIC (anti-plant pathogens) was 6.25 μM[58]
A. creber EN-602versiamide A (26), 3, 15-dehydroprotuboxepin K (27)MIC (anti-bacteria) was 8–64 μg/mL[59]
Aspergillus sp. RR-YLW12terretonin F (28)IC50 (anti-three microalgae) were 3.1, 5.2, 10.5 μg/mL[60]
Marine corals
A. hiratsukae SCSIO 5Bn1003demethylincisterol A2 (29), asperophiobolin E (30),
butyrolactone I (31)		MIC (anti-B. subtilis) were 10.26 ± 0.76, 17.00 ± 1.25 and 5.30 ± 0.29 μM[61]
A. hiratsukae SCSIO 7S2001methterpenoids H-L (32–36) neoechinulin A (37)MIC (anti-bacteria) was 6.25–100 μg/mL[62]
A. terreus SCSIO41404versicolactone B (38),
butyrolactone VI (39)		IC50 (anti-E. faecalis, K. pneumoniae) were 25 and 50 μg/mL[63]
A. unguis GXIMD 0250540–45MIC (anti-bacteria) was 2–64 μg/mL[64]
Aspergillus sp. SCSIO 41501maribasins C–E,A,B (46–50)MIC (anti-plant pathogens) was 3.12–50 μg/disc[34]
Sponges
A. candius KUFA 0062preussin (51)anti-pathogens[65]
A. flavipes KUFA1152aspulvinones B’, H, R and S (52–55)MIC (anti-pathogens) was 16–64 μg/mL[66]
A. niger L14fonsecinone A (56),
isoaurasperone A (57)		MIC (anti-H. pylori) was ≤4 μg/mL[67]
A. ochraceopetaliformis SCSIO 41018hydroxy-neotriamycin (58)MIC (anti-pathogens) was 0.45–7.8 μg/mL μM[68]
A. terreus 164018aspergetherins A, C (59, 60)
3, 5-dichloroasterric acid (61), methyl chloroasterrate (62)		MIC (anti-MRSA) was 1.0–128 μg/mL[69]
Aspergillus sp. LS57aspergilluone A (63)MIC (anti-pathogens) was 32–128 μg/mL[70]
Aspergillus sp. LS116perinadines B, C (64, 65)MIC (anti-B. subtilis) were 32 and 64 μg/mL[71]
Seawater
A. fumigatus H2212,13-dihydroxyfumitremorgin C (66),
fumitremorgin B (67)		MIC(anti-M. Bovis, C. albicans) were 25 and 50 μM[72]
A. fumigatus H22(66),13-oxofumitremorgin B (68)antibacterial activity[72]
A. fumigatus H22fumagillin (69),
helvolic acid (70), 6-O-propionyl-16-O-deacetylhelvolic acid (71), 16-O-propionyl-6-O-deacetylhelvolic acid (72), penibenzophenone E (73), sulochrin (74)		MIC (anti-MRSA) were 1.25 and 2.5[72]
A. unguisunguidepside C (75), aspersidone B (76), agonodepside C (77)MIC (anti-bacteria) was 5.3 to 22.1 μM[73]
A. aculeatinus WHUF0198aculeaxanthone A (78)MIC (anti-bacteria) was 1.0 to 4.0 μM[74]
Marine sediments
A. flavus SCSIO F025cyclopiamide (79), speradines G,H,B,C (80–83), CPA (84)weak anti-bacteria[75]
A. fumigatus SD-40685–90MIC (anti-bacteria and plant pathogens) were 4–64 μg/mL[76]
Aspergillus sp. CSYZ-1meroterpenoid (91)MIC (anti-S. aureus, H. pylori) were 2–16 and 1–4 μg/mL[77]
Aspergillus sp. IMCASMF180035aspergiloxathene A (92)MIC (anti-MRSA, S. aureus) were 22.40 and 5.60 μM[30]
Aspergillus sp. IMCASMF180035Δ2′-1′-dehydropenicillide (93), dehydropenicillide (94)MIC (anti-H. pylori) were 21.61 and 21.73 μM[30]
Aspergillus sp. YJ191021asperthrins A (95)MIC (anti-plant pathogens) was 8–25μg/mL[78]
Aspergillus sp. WHUF052366, 8-di-O-methylversicolorin A (96), 6,8,1′-tri-O-methylaverantin (97),
6,8-di-O-methylaverantin (98)		MIC (anti-H. pylori) was 20.00 to 43.47 μM[79]
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Li, H.; Fu, Y.; Song, F. Marine Aspergillus: A Treasure Trove of Antimicrobial Compounds. Mar. Drugs 2023, 21, 277. https://doi.org/10.3390/md21050277

AMA Style

Li H, Fu Y, Song F. Marine Aspergillus: A Treasure Trove of Antimicrobial Compounds. Marine Drugs. 2023; 21(5):277. https://doi.org/10.3390/md21050277

Chicago/Turabian Style

Li, Honghua, Yanqi Fu, and Fuhang Song. 2023. "Marine Aspergillus: A Treasure Trove of Antimicrobial Compounds" Marine Drugs 21, no. 5: 277. https://doi.org/10.3390/md21050277

APA Style

Li, H., Fu, Y., & Song, F. (2023). Marine Aspergillus: A Treasure Trove of Antimicrobial Compounds. Marine Drugs, 21(5), 277. https://doi.org/10.3390/md21050277

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