Next Article in Journal
Evaluation of Phytochemical Screening, Pigment Content, In Vitro Antioxidant, Antibacterial Potential and GC-MS Metabolite Profiling of Green Seaweed Caulerpa racemosa
Next Article in Special Issue
Cytosporin Derivatives from Arctic-Derived Fungus Eutypella sp. D-1 via the OSMAC Approach
Previous Article in Journal
Development of a Sequential Fractionation-and-Recovery Method for Multiple Anti-Inflammatory Components Contained in the Dried Red Alga Dulse (Palmaria palmata)
Previous Article in Special Issue
Chemomodulatory Effect of the Marine-Derived Metabolite “Terrein” on the Anticancer Properties of Gemcitabine in Colorectal Cancer Cells
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Marine Drugs
Volume 21
Issue 5
10.3390/md21050277
marinedrugs-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
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)
Browse Figures
Versions Notes

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.

References

  1. Li, C.S.; Liu, L.T.; Yang, L.; Li, J.; Dong, X. Chemistry and bioactivity of marine-derived bisabolane sesquiterpenoids: A review. Front. Chem. 2022, 10, 881767. [Google Scholar] [CrossRef] [PubMed]
  2. Carroll, A.R.; Copp, B.R.; Davis, R.A.; Keyzers, R.A.; Prinsep, M.R. Marine natural products. Nat. Prod. Rep. 2020, 37, 175–223. [Google Scholar] [CrossRef]
  3. Liu, L.L.; Wu, C.H.; Qian, P.Y. Marine natural products as antifouling molecules—A mini-review (2014–2020). Biofouling 2020, 36, 1210–1226. [Google Scholar] [CrossRef] [PubMed]
  4. Cardoso, J.; Nakayama, D.G.; Sousa, E.; Pinto, E. Marine-derived compounds and prospects for their antifungal application. Molecules 2020, 25, 5856. [Google Scholar] [CrossRef]
  5. Bian, C.; Wang, J.; Zhou, X.; Wu, W.; Guo, R. Recent advances on marine alkaloids from sponges. Chem. Biodivers. 2020, 17, e2000186. [Google Scholar] [CrossRef]
  6. Ge, X.; Wang, Y.; Sun, C.; Zhang, Z.; Song, L.; Tan, L.; Li, D.; Yang, S.; Yu, G. Secondary metabolites produced by coculture of Pleurotus ostreatus SY10 and Pleurotus eryngii SY302. Chem. Biodivers. 2022, 19, e202100832. [Google Scholar] [CrossRef] [PubMed]
  7. Li, K.; Chen, S.; Pang, X.; Cai, J.; Zhang, X.; Liu, Y.; Zhu, Y.; Zhou, X. Natural products from mangrove sediments-derived microbes: Structural diversity, bioactivities, biosynthesis, and total synthesis. Eur. J. Med. Chem. 2022, 230, 114117. [Google Scholar] [CrossRef]
  8. Wiese, J.; Imhoff, J.F. Marine bacteria and fungi as promising source for new antibiotics. Drug Dev. Res. 2019, 80, 24–27. [Google Scholar] [CrossRef] [Green Version]
  9. Wang, H.N.; Sun, S.S.; Liu, M.Z.; Yan, M.C.; Liu, Y.F.; Zhu, Z.; Zhang, Z. Natural bioactive compounds from marine fungi (2017–2020). J. Asian Nat. Prod. Res. 2022, 24, 203–230. [Google Scholar] [CrossRef]
  10. Rani, A.; Saini, K.C.; Bast, F.; Varjani, S.; Mehariya, S.; Bhatia, S.K.; Sharma, N.; Funk, C. A review on microbial products and their perspective application as antimicrobial agents. Biomolecules 2021, 11, 1860. [Google Scholar] [CrossRef]
  11. Wang, W.; Gao, M.; Luo, Z.; Liao, Y.; Zhang, B.; Ke, W.; Shao, Z.; Li, F.; Chen, J. Secondary metabolites isolated from the deep sea-derived fungus Aspergillus sydowii C1-S01-A7. Nat. Prod. Res. 2019, 33, 3077–3082. [Google Scholar] [CrossRef] [PubMed]
  12. Chen, G.; Wang, H.F.; Pei, Y.H. Secondary metabolites from marine-derived microorganisms. J. Asian Nat. Prod. Res. 2014, 16, 105–122. [Google Scholar] [CrossRef] [PubMed]
  13. Julianti, E.; Abrian, I.A.; Wibowo, M.S.; Azhari, M.; Tsurayya, N.; Izzati, F.; Juanssilfero, A.B.; Bayu, A.; Rahmawati, S.I.; Putra, M.Y. Secondary metabolites from marine-derived fungi and actinobacteria as potential sources of novel colorectal cancer drugs. Mar. Drugs 2022, 20, 67. [Google Scholar] [CrossRef] [PubMed]
  14. Chen, S.; Cai, R.; Liu, Z.; Cui, H.; She, Z. Secondary metabolites from mangrove-associated fungi: Source, chemistry and bioactivities. Nat. Prod. Rep. 2021, 39, 560–595. [Google Scholar] [CrossRef]
  15. Chen, Y.; Pang, X.; He, Y.; Lin, X.; Zhou, X.; Liu, Y.; Yang, B. Secondary metabolites from coral-associated fungi: Source, chemistry and bioactivities. J. Fungi 2022, 8, 1043. [Google Scholar] [CrossRef]
  16. Liu, Z.; Zhao, J.-Y.; Sun, S.-F.; Li, Y.; Liu, Y.-B. Fungi: Outstanding source of novel chemical scaffolds. J. Asian Nat. Prod. Res. 2018, 22, 99–120. [Google Scholar] [CrossRef]
  17. Schueffler, A.; Anke, T. Fungal natural products in research and development. Nat. Prod. Rep. 2014, 31, 1425–1448. [Google Scholar] [CrossRef]
  18. Dell’Anno, F.; Rastelli, E.; Buschi, E.; Barone, G.; Beolchini, F.; Dell’Anno, A. Fungi can be more effective than bacteria for the bioremediation of marine sediments highly contaminated with heavy metals. Microorganisms 2022, 10, 993. [Google Scholar] [CrossRef]
  19. Jiang, M.; Wu, Z.; Guo, H.; Liu, L.; Chen, S. A review of terpenes from marine-derived fungi: 2015–2019. Mar. Drugs 2020, 18, 321. [Google Scholar] [CrossRef]
  20. Wali, A.F.; Majid, S.; Rasool, S.; Shehada, S.B.; Abdulkareem, S.K.; Firdous, A.; Beigh, S.; Shakeel, S.; Mushtaq, S.; Akbar, I.; et al. Natural products against cancer: Review on phytochemicals from marine sources in preventing cancer. Saudi Pharm. J. 2019, 27, 767–777. [Google Scholar] [CrossRef]
  21. Qadri, H.; Shah, A.H.; Ahmad, S.M.; Alshehri, B.; Almilaibary, A.; Mir, M.A. Natural products and their semi-synthetic derivatives against antimicrobial-resistant human pathogenic bacteria and fungi. Saudi J. Biol. Sci. 2022, 29, 103376. [Google Scholar] [CrossRef] [PubMed]
  22. Youssef, F.S.; Ashour, M.L.; Singab, A.N.B.; Wink, M. A comprehensive review of bioactive peptides from marine fungi and their biological significance. Mar. Drugs 2019, 17, 559. [Google Scholar] [CrossRef] [Green Version]
  23. Qi, J.; Chen, C.; He, Y.; Wang, Y. Genomic analysis and antimicrobial components of M7, an Aspergillus terreus strain derived from the south china sea. J. Fungi 2022, 8, 1051. [Google Scholar] [CrossRef] [PubMed]
  24. Mia, M.M.; Hasan, M.; Miah, M.M.; Hossain, M.A.S.; Islam, S.; Shanta, V. Inhibitory potentiality of secondary metabolites extracted from marine fungus target on avian influenza virus-a subtype H5N8 (Neuraminidase) and H5N1 (Nucleoprotein): A rational virtual screening. Vet. Anim. Sci. 2022, 15, 100231. [Google Scholar]
  25. Fan, M.; Nath, A.K.; Tang, Y.; Choi, Y.-J.; Debnath, T.; Choi, E.-J.; Kim, E.-K. Investigation of the anti-prostate cancer properties of marine-derived compounds. Mar. Drugs 2018, 16, 160. [Google Scholar] [CrossRef] [Green Version]
  26. Zhao, H.; Ji, R.; Zha, X.; Xu, Z.; Lin, Y.; Zhou, S. Investigation of the bactericidal mechanism of Penicilazaphilone C on Escherichia coli based on 4D label-free quantitative proteomic analysis. Eur. J. Pharm. Sci. 2022, 179, 106299. [Google Scholar] [CrossRef] [PubMed]
  27. Xu, X.; Han, J.; Zhang, X.; Xu, W.; Yang, J.; Song, F. Investigation on the chemical constituents of the marine-derived fungus strain Aspergillus brunneoviolaceus MF180246. Nat. Prod. Res. 2022, 1–6. [Google Scholar] [CrossRef] [PubMed]
  28. Barzkar, N.; Sheng, R.; Sohail, M.; Jahromi, S.T.; Babich, O.; Sukhikh, S.; Nahavandi, R. Alginate lyases from marine bacteria: An enzyme ocean for sustainable future. Molecules 2022, 27, 3375. [Google Scholar] [CrossRef] [PubMed]
  29. Willems, T.; De Mol, M.L.; De Bruycker, A.; De Maeseneire, S.L.; Soetaert, W.K. Alkaloids from marine fungi: Promising antimicrobials. Antibiotics 2020, 9, 340. [Google Scholar] [CrossRef] [PubMed]
  30. Song, F.; Lin, R.; Yang, N.; Jia, J.; Wei, S.; Han, J.; Li, J.; Bi, H.; Xu, X. Antibacterial secondary metabolites from marine-derived fungus Aspergillus sp. IMCASMF180035. Antibiotics 2021, 10, 377. [Google Scholar] [CrossRef]
  31. Nweze, J.A.; Mbaoji, F.N.; Huang, G.; Li, Y.; Yang, L.; Zhang, Y.; Huang, S.; Pan, L.; Yang, D. Antibiotics development and the potentials of marine-derived compounds to stem the tide of multidrug-resistant pathogenic bacteria, fungi, and protozoa. Mar. Drugs 2020, 18, 145. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  32. Chu, Y.C.; Chang, C.H.; Liao, H.R.; Fu, S.L.; Chen, J.J. Anti-cancer and anti-inflammatory activities of three new chromone derivatives from the marine-derived Penicillium citrinum. Mar. Drugs 2021, 19, 408. [Google Scholar] [CrossRef] [PubMed]
  33. Thawabteh, A.M.; Swaileh, Z.; Ammar, M.; Jaghama, W.; Yousef, M.; Karaman, R.; Bufo, S.A.; Scrano, L. Antifungal and antibacterial activities of isolated marine compounds. Toxins 2023, 15, 93. [Google Scholar] [CrossRef] [PubMed]
  34. Yao, F.-H.; Liang, X.; Cheng, X.; Ling, J.; Dong, J.-D.; Qi, S.-H. Antifungal peptides from the marine gorgonian-associated fungus Aspergillus sp. SCSIO41501. Phytochemistry 2021, 192, 112967. [Google Scholar] [CrossRef]
  35. Sweilam, S.H.; Alqarni, M.H.; Youssef, F.S.; Noureini, S.K. Antimicrobial alkaloids from marine-derived fungi as drug leads versus COVID-19 infection: A computational approach to explore their anti-COVID-19 activity and ADMET properties. Evid.-Based Complement. Altern. Med. 2022, 2022, 1–19. [Google Scholar] [CrossRef]
  36. Abuhijjleh, R.K.; Shabbir, S.; Al-Abd, A.M.; Jiaan, N.H.; Alshamil, S.; El-labbad, E.M.; Khalifa, S.I. Bioactive marine metabolites derived from the Persian Gulf compared to the Red Sea: Similar environments and wide gap in drug discovery. PeerJ 2021, 9, e11778. [Google Scholar] [CrossRef]
  37. Giri, A.; Ohshima, T. Bioactive marine peptides: Nutraceutical value and novel approaches. Adv. Food Nutr. Res. 2012, 65, 73–105. [Google Scholar] [CrossRef]
  38. Elissawy, A.M.; El-Shazly, M.; Ebada, S.S.; Singab, A.B.; Proksch, P. Bioactive terpenes from marine-derived fungi. Mar. Drugs 2015, 13, 1966–1992. [Google Scholar] [CrossRef] [Green Version]
  39. Jiang, M.; Chen, S.; Li, J.; Liu, L. The biological and chemical diversity of tetramic acid compounds from marine-derived microorganisms. Mar. Drugs 2020, 18, 114. [Google Scholar] [CrossRef] [Green Version]
  40. Fouillaud, M.; Venkatachalam, M.; Girard-Valenciennes, E.; Caro, Y.; Dufosse, L. Anthraquinones and derivatives from marine-derived fungi: Structural diversity and selected biological activities. Mar. Drugs 2016, 14, 64. [Google Scholar] [CrossRef] [Green Version]
  41. Hafez Ghoran, S.; Taktaz, F.; Ayatollahi, S.A.; Kijjoa, A. Anthraquinones and their analogues from marine-derived fungi: Chemistry and biological activities. Mar. Drugs 2022, 20, 474. [Google Scholar] [CrossRef] [PubMed]
  42. Li, Y.X.; Himaya, S.W.; Kim, S.K. Triterpenoids of marine origin as anti-cancer agents. Molecules 2013, 18, 7886–7909. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  43. Wang, K.W.; Ding, P. New bioactive metabolites from the marine-derived fungi Aspergillus. Mini-Rev. Med. Chem. 2018, 18, 1072–1094. [Google Scholar] [CrossRef] [PubMed]
  44. Xu, K.; Yuan, X.L.; Li, C.; Li, A.X. Recent discovery of heterocyclic alkaloids from marine-derived Aspergillus species. Mar. Drugs 2020, 18, 54. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  45. Al-Rajhi, A.M.H.; Mashraqi, A.; Al Abboud, M.A.; Shater, A.M.; Al Jaouni, S.K.; Selim, S.; Abdelghany, T.M. Screening of bioactive compounds from endophytic marine-derived fungi in saudi arabia: Antimicrobial and anticancer potential. Life 2022, 12, 1182. [Google Scholar] [CrossRef]
  46. Liu, C.C.; Zhang, Z.Z.; Feng, Y.Y.; Gu, Q.Q.; Li, D.H.; Zhu, T.J. Secondary metabolites from antarctic marine-derived fungus Penicillium crustosum HDN153086. Nat. Prod. Res. 2019, 33, 414–419. [Google Scholar] [CrossRef]
  47. Zheng, Y.Y.; Ma, Z.L.; Wu, J.S.; Shao, C.L.; Yao, G.S.; Wang, C.Y. Induction of secondary metabolite biosynthesis by deleting the histone deacetylase HdaA in the marine-derived fungus Aspergillus terreus RA2905. J. Fungi 2022, 8, 1024. [Google Scholar] [CrossRef]
  48. Zhang, K.; Zhang, X.; Lin, R.; Yang, H.; Song, F.; Xu, X.; Wang, L. New secondary metabolites from the marine-derived fungus Talaromyces mangshanicus BTBU20211089. Mar. Drugs 2022, 20, 79. [Google Scholar] [CrossRef]
  49. Zaman, K.A.U.; Wu, X.; Sarotti, A.M.; Cao, S. New and bioactive polyketides from Hawaiian marine-derived fungus Trichoderma sp. FM652. Nat. Prod. Res. 2022, 36, 5984–5990. [Google Scholar] [CrossRef]
  50. Xie, M.M.; Jiang, J.Y.; Zou, Z.B.; Xu, L.; Zhang, Y.; Wang, C.F.; Liu, C.B.; Yan, Q.X.; Liu, Z.; Yang, X.W. Chemical constituents of the deep-sea-derived fungus Cladosporium oxysporum 170103 and their antibacterial effects. Chem. Biodivers. 2022, 19, e202200963. [Google Scholar] [CrossRef]
  51. Wang, Y.; Chen, W.; Xu, Z.; Bai, Q.; Zhou, X.; Zheng, C.; Bai, M.; Chen, G. Biological secondary metabolites from the lumnitzera littorea-derived fungus Penicillium oxalicum HLLG-13. Mar. Drugs 2022, 21, 22. [Google Scholar] [CrossRef] [PubMed]
  52. Xu, X.; Guo, S.; Chen, H.; Zhang, Z.; Li, X.; Wang, W.; Guo, L. Bioassay-guided isolation and characterization of antibacterial compound from Aspergillus fumigatus HX-1 associated with Clam. 3 Biotech 2021, 11, 193. [Google Scholar] [CrossRef] [PubMed]
  53. Youssef, D.T.A.; Shaala, L.A.; Genta-Jouve, G. Asperopiperazines A and B: Antimicrobial and cytotoxic dipeptides from a tunicate-derived fungus Aspergillus sp. DY001. Mar. Drugs 2022, 20, 451. [Google Scholar] [CrossRef] [PubMed]
  54. Hu, Z.; Zhu, Y.; Chen, J.; Chen, J.; Li, C.; Gao, Z.; Li, J.; Liu, L. Sesquiterpenoids with phytotoxic and antifungal activities from a pathogenic fungus Aspergillus alabamensis. J. Agric. Food Chem. 2022, 70, 12065–12073. [Google Scholar] [CrossRef]
  55. Hu, Z.; Zhu, Y.; Chen, J.; Chen, J.; Li, C.; Gao, Z.; Li, J.; Liu, L. Discovery of novel bactericides from Aspergillus alabamensis and their antibacterial activity against fish pathogens. J. Agric. Food Chem. 2023, 71, 4298–4305. [Google Scholar] [CrossRef]
  56. Zhou, G.; Zhang, X.; Shah, M.; Che, Q.; Zhang, G.; Gu, Q.; Zhu, T.; Li, D. Polyhydroxy p-terphenyls from a mangrove endophytic fungus Aspergillus candidus LDJ-5. Mar. Drugs 2021, 19, 82. [Google Scholar] [CrossRef]
  57. Zang, Z.; Yang, W.; Cui, H.; Cai, R.; Li, C.; Zou, G.; Wang, B.; She, Z. Two antimicrobial heterodimeric tetrahydroxanthones with a 7,7′-linkage from mangrove endophytic fungus Aspergillus flavus QQYZ. Molecules 2022, 27, 2691. [Google Scholar] [CrossRef]
  58. Lin, L.-B.; Gao, Y.-Q.; Han, R.; Xiao, J.; Wang, Y.-M.; Zhang, Q.; Zhai, Y.-J.; Han, W.-B.; Li, W.-L.; Gao, J.-M. Alkylated salicylaldehydes and prenylated indole alkaloids from the endolichenic fungus Aspergillus chevalieri and their bioactivities. J. Agric. Food Chem. 2021, 69, 6524–6534. [Google Scholar] [CrossRef]
  59. Li, H.-L.; Yang, S.-Q.; Li, X.-M.; Li, X.; Wang, B.-G. Structurally diverse alkaloids produced by Aspergillus creber EN-602, an endophytic fungus obtained from the marine red alga Rhodomela confervoides. Bioorg. Chem. 2021, 110, 104822. [Google Scholar] [CrossRef]
  60. Fang, S.-T.; Liu, X.-H.; Yan, B.-F.; Miao, F.-P.; Yin, X.-L.; Li, W.-Z.; Ji, N.-Y. Terpenoids from the marine-derived fungus Aspergillus sp. RR-YLW-12, associated with the red alga Rhodomela confervoides. J. Nat. Prod. 2021, 84, 1763–1771. [Google Scholar] [CrossRef]
  61. Zeng, Q.; Chen, Y.; Wang, J.; Shi, X.; Che, Y.; Chen, X.; Zhong, W.; Zhang, W.; Wei, X.; Wang, F.; et al. Diverse secondary metabolites from the coral-derived fungus Aspergillus hiratsukae SCSIO 5Bn1003. Mar. Drugs 2022, 20, 150. [Google Scholar] [CrossRef] [PubMed]
  62. Chen, X.Y.; Zeng, Q.; Chen, Y.C.; Zhong, W.M.; Xiang, Y.; Wang, J.F.; Shi, X.F.; Zhang, W.M.; Zhang, S.; Wang, F.Z. Chevalones H-M: Six new alpha-pyrone meroterpenoids from the gorgonian coral-derived fungus Aspergillus hiratsukae SCSIO 7S2001. Mar. Drugs 2022, 20, 71. [Google Scholar] [CrossRef] [PubMed]
  63. Peng, Q.; Chen, W.; Lin, X.; Xiao, J.; Liu, Y.; Zhou, X. Butenolides from the coral-derived fungus Aspergillius terreus SCSIO41404. Mar. Drugs 2022, 20, 212. [Google Scholar] [CrossRef] [PubMed]
  64. Zhang, Y.; Li, Z.; Huang, B.; Liu, K.; Peng, S.; Liu, X.; Gao, C.; Liu, Y.; Tan, Y.; Luo, X. Anti-osteoclastogenic and antibacterial effects of chlorinated polyketides from the Beibu gulf coral-derived fungus Aspergillus unguis GXIMD 02505. Mar. Drugs 2022, 20, 178. [Google Scholar] [CrossRef] [PubMed]
  65. Buttachon, S.; Ramos, A.A.; Inacio, A.; Dethoup, T.; Gales, L.; Lee, M.; Costa, P.M.; Silva, A.M.S.; Sekeroglu, N.; Rocha, E.; et al. Bis-indolyl benzenoids, hydroxypyrrolidine derivatives and other constituents from cultures of the marine sponge-associated fungus Aspergillus candidus KUFA. Mar. Drugs 2018, 16, 119. [Google Scholar] [CrossRef] [Green Version]
  66. Machado, F.P.; Kumla, D.; Pereira, J.A.; Sousa, E.; Dethoup, T.; Freitas-Silva, J.; Costa, P.M.; Mistry, S.; Silva, A.M.S.; Kijjoa, A. Prenylated phenylbutyrolactones from cultures of a marine sponge-associated fungus Aspergillus flavipes KUFA1152. Phytochemistry 2021, 185, 112709. [Google Scholar] [CrossRef]
  67. Liu, J.; Yu, R.; Jia, J.; Gu, W.; Zhang, H. Assignment of absolute configurations of two promising anti-helicobacter pylori agents from the marine sponge-derived fungus Aspergillus niger L14. Molecules 2021, 26, 5061. [Google Scholar] [CrossRef]
  68. Guo, C.; Wang, P.; Pang, X.; Lin, X.; Liao, S.; Yang, B.; Zhou, X.; Wang, J.; Liu, Y. Discovery of a dimeric zinc complex and five cyclopentenone derivatives from the sponge-associated fungus Aspergillus ochraceopetaliformis. ACS Omega 2021, 6, 8942–8949. [Google Scholar] [CrossRef]
  69. Li, J.X.; Xu, Q.H.; Shang, R.Y.; Liu, Q.; Luo, X.C.; Lin, H.W.; Jiao, W.H. Aspergetherins A-D, new chlorinated biphenyls with anti-MRSA activity from the marine sponge symbiotic fungus Aspergillus terreus 164018. Chem. Biodivers. 2023, e202300010. [Google Scholar] [CrossRef]
  70. Liu, Y.; Ding, L.; He, J.; Zhang, Z.; Deng, Y.; He, S.; Yan, X. A new antibacterial chromone from a marine sponge-associated fungus Aspergillus sp. LS57. Fitoterapia 2021, 154, 105004. [Google Scholar] [CrossRef]
  71. Liu, Y.; Ding, L.; Shi, Y.; Yan, X.; Wu, B.; He, S. Molecular networking-driven discovery of antibacterial perinadines, new tetracyclic alkaloids from the marine sponge-derived fungus Aspergillus sp. ACS Omega 2022, 7, 9909–9916. [Google Scholar] [CrossRef] [PubMed]
  72. Zhang, R.; Wang, H.; Chen, B.; Dai, H.; Sun, J.; Han, J.; Liu, H. Discovery of anti-MRSA secondary metabolites from a marine-derived fungus Aspergillus fumigatus. Mar. Drugs 2022, 20, 302. [Google Scholar] [CrossRef] [PubMed]
  73. Anh, C.V.; Kwon, J.-H.; Kang, J.S.; Lee, H.-S.; Heo, C.-S.; Shin, H.J. Antibacterial and cytotoxic phenolic polyketides from two marine-derived fungal strains of Aspergillus unguis. Pharmaceuticals 2022, 15, 74. [Google Scholar] [CrossRef]
  74. Wu, J.; Shui, H.; Zhang, M.; Zeng, Y.; Zheng, M.; Zhu, K.K.; Wang, S.B.; Bi, H.; Hong, K.; Cai, Y.S. Aculeaxanthones A-E, new xanthones from the marine-derived fungus Aspergillus aculeatinus WHUF0198. Front. Microbiol. 2023, 14, 1138830. [Google Scholar] [CrossRef]
  75. Xiang, Y.; Zeng, Q.; Mai, Z.-M.; Chen, Y.-C.; Shi, X.-F.; Chen, X.-Y.; Zhong, W.-M.; Wei, X.-Y.; Zhang, W.-M.; Zhang, S.; et al. Asperorydines N-P, three new cyclopiazonic acid alkaloids from the marine-derived fungus Aspergillus flavus SCSIO F025. Fitoterapia 2021, 150, 104839. [Google Scholar] [CrossRef]
  76. Yan, L.-H.; Li, X.-M.; Chi, L.-P.; Li, X.; Wang, B.-G. Six new antimicrobial metabolites from the deep-sea sediment-derived fungus Aspergillus fumigatus SD-406. Mar. Drugs 2021, 20, 4. [Google Scholar] [CrossRef]
  77. Cen, S.; Jia, J.; Ge, Y.; Ma, Y.; Li, X.; Wei, J.; Bai, Y.; Wu, X.; Song, J.; Bi, H.; et al. A new antibacterial 3,5-dimethylorsellinic acid-based meroterpene from the marine fungus Aspergillus sp. CSYZ-1. Fitoterapia 2021, 152, 104908. [Google Scholar] [CrossRef]
  78. Yang, J.; Gong, L.; Guo, M.; Jiang, Y.; Ding, Y.; Wang, Z.; Xin, X.; An, F. Bioactive indole diketopiperazine alkaloids from the marine endophytic fungus Aspergillus sp. YJ191021. Mar. Drugs 2021, 19, 157. [Google Scholar] [CrossRef]
  79. Lv, H.; Zhang, J.; Xue, Y.; Li, S.; Sun, X.; Jia, J.; Bi, H.; Wang, S.; Su, H.; Zhu, M.; et al. Two new austocystin analogs from the marine-derived fungus Aspergillus sp. WHUF05236. Chem. Biodivers. 2022, 19, e202200207. [Google Scholar] [CrossRef]
  80. Quang, T.H.; Phong, N.V.; Anh, L.N.; Hanh, T.T.H.; Cuong, N.X.; Ngan, N.T.T.; Trung, N.Q.; Nam, N.H.; Minh, C.V. Secondary metabolites from a peanut-associated fungus Aspergillus niger IMBC-NMTP01 with cytotoxic, anti-inflammatory, and antimicrobial activities. Nat. Prod. Res. 2022, 36, 1215–1223. [Google Scholar] [CrossRef]
  81. Tian, Y.; Li, Y. A review on bioactive compounds from marine-derived chaetomium species. J. Microbiol. Biotechnol. 2022, 32, 541–550. [Google Scholar] [CrossRef] [PubMed]
  82. Xu, J.; Yi, M.; Ding, L.; He, S. A review of anti-inflammatory compounds from marine fungi, 2000–2018. Mar. Drugs 2019, 17, 636. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  83. Sun, L.; Wang, H.; Yan, M.; Sai, C.; Zhang, Z. Research advances of bioactive sesquiterpenoids isolated from marine-derived Aspergillus sp. Molecules 2022, 27, 7376. [Google Scholar] [CrossRef] [PubMed]
  84. Arockianathan, P.M.; Mishra, M.; Niranjan, R. Recent status and advancements in the development of antifungal agents: Highlights on plant and marine based antifungals. Curr. Top. Med. Chem. 2019, 19, 812–830. [Google Scholar] [CrossRef]
  85. Sharma, D.; Bisht, G.S. Recent updates on antifungal peptides. Mini-Rev. Med. Chem. 2020, 20, 260–268. [Google Scholar] [CrossRef]
  86. Montuori, E.; de Pascale, D.; Lauritano, C. Recent discoveries on marine organism immunomodulatory activities. Mar. Drugs 2022, 20, 422. [Google Scholar] [CrossRef]
  87. Hou, X.; Zhang, X.; Xue, M.; Zhao, Z.; Zhang, H.; Xu, D.; Lai, D.; Zhou, L. Recent advances in sorbicillinoids from fungi and their bioactivities (Covering 2016–2021). J. Fungi 2022, 8, 62. [Google Scholar] [CrossRef]
  88. Lima, R.N.; Porto, A.L.M. Recent advances in marine enzymes for biotechnological processes. Adv. Food Nutr. Res. 2016, 78, 153–192. [Google Scholar]
  89. Wang, Y.-N.; Meng, L.-H.; Wang, B.-G. Progress in research on bioactive secondary metabolites from deep-sea derived microorganisms. Mar. Drugs 2020, 18, 614. [Google Scholar] [CrossRef]
  90. Hang, S.; Chen, H.; Wu, W.; Wang, S.; Fang, Y.; Sheng, R.; Tu, Q.; Guo, R. Progress in isoindolone alkaloid derivatives from marine microorganism: Pharmacology, preparation, and mechanism. Mar. Drugs 2022, 20, 405. [Google Scholar] [CrossRef]
  91. Yang, X.; Liu, J.; Mei, J.; Jiang, R.; Tu, S.; Deng, H.; Liu, J.; Yang, S.; Li, J. Origins, structures, and bioactivities of secondary metabolites from marine-derived Penicillium fungi. Mini-Rev. Med. Chem. 2021, 21, 2000–2019. [Google Scholar] [CrossRef] [PubMed]
  92. Li, X.; Xu, J.; Wang, P.; Ding, W. Novel indole diketopiperazine stereoisomers from a marine-derived fungus Aspergillus sp. Mycology 2023, 14, 1–10. [Google Scholar] [CrossRef] [PubMed]
  93. Zhao, L.; Lin, X.; Fu, J.; Zhang, J.; Tang, W.; He, Z. A novel bi-functional fibrinolytic enzyme with anticoagulant and thrombolytic activities from a marine-derived fungus Aspergillus versicolor ZLH-1. Mar. Drugs 2022, 20, 356. [Google Scholar] [CrossRef] [PubMed]
  94. Xu, J.; Liu, P.; Li, X.; Gan, L.; Wang, P. Novel stemphol derivatives from a marine fungus Pleospora sp. Nat. Prod. Res. 2018, 33, 367–373. [Google Scholar] [CrossRef]
  95. Song, Z.; Gao, J.; Hu, J.; He, H.; Huang, P.; Zhang, L.; Song, F. One new xanthenone from the marine-derived fungus Aspergillus versicolor MF160003. Nat. Prod. Res. 2020, 34, 2907–2912. [Google Scholar] [CrossRef]
  96. Wu, J.S.; Shi, X.H.; Yao, G.S.; Shao, C.L.; Fu, X.M.; Zhang, X.L.; Guan, H.S.; Wang, C.Y. New thiodiketopiperazine and 3,4-dihydroisocoumarin derivatives from the marine-derived fungus Aspergillus terreus. Mar. Drugs 2020, 18, 132. [Google Scholar] [CrossRef] [Green Version]
  97. Xu, Y.; Huang, R.; Liu, H.; Yan, T.; Ding, W.; Jiang, Y.; Wang, P.; Zheng, D.; Xu, J. New polyketides from the marine-derived fungus Letendraea Sp. 5XNZ4-2. Mar. Drugs 2019, 18, 18. [Google Scholar] [CrossRef] [Green Version]
  98. Xu, X.; Li, J.; Zhang, K.; Wei, S.; Lin, R.; Polyak, S.W.; Yang, N.; Song, F. New isocoumarin analogues from the marine-derived fungus Paraphoma sp. CUGBMF180003. Mar. Drugs 2021, 19, 313. [Google Scholar] [CrossRef]
  99. Hu, J.; Li, Z.; Gao, J.; He, H.; Dai, H.; Xia, X.; Liu, C.; Zhang, L.; Song, F. New diketopiperazines from a marine-derived fungus strain Aspergillus versicolor MF180151. Mar. Drugs 2019, 17, 262. [Google Scholar] [CrossRef] [Green Version]
Marinedrugs 21 00277 g001 550
Figure 1. Compounds of Aspergillus sp. derived from marine animals.
Figure 1. Compounds of Aspergillus sp. derived from marine animals.
Marinedrugs 21 00277 g001
Marinedrugs 21 00277 g002 550
Figure 2. Compounds of Aspergillus sp. derived from marine plants.
Figure 2. Compounds of Aspergillus sp. derived from marine plants.
Marinedrugs 21 00277 g002
Marinedrugs 21 00277 g003 550
Figure 3. Compounds of Aspergillus sp. derived from mangroves.
Figure 3. Compounds of Aspergillus sp. derived from mangroves.
Marinedrugs 21 00277 g003
Marinedrugs 21 00277 g004 550
Figure 4. Compounds of Aspergillus sp. derived from algae.
Figure 4. Compounds of Aspergillus sp. derived from algae.
Marinedrugs 21 00277 g004
Marinedrugs 21 00277 g005 550
Figure 5. Compounds of Aspergillus sp. derived from corals.
Figure 5. Compounds of Aspergillus sp. derived from corals.
Marinedrugs 21 00277 g005
Marinedrugs 21 00277 g006 550
Figure 6. Compounds of Aspergillus sp. derived from sponges.
Figure 6. Compounds of Aspergillus sp. derived from sponges.
Marinedrugs 21 00277 g006
Marinedrugs 21 00277 g007 550
Figure 7. Compounds of Aspergillus sp. derived from seawater.
Figure 7. Compounds of Aspergillus sp. derived from seawater.
Marinedrugs 21 00277 g007
Marinedrugs 21 00277 g008 550
Figure 8. Compounds of Aspergillus sp. derived from marine sediments.
Figure 8. Compounds of Aspergillus sp. derived from marine sediments.
Marinedrugs 21 00277 g008
Marinedrugs 21 00277 g009 550
Figure 9. The proportion of Aspergillus from different marine sources.
Figure 9. The proportion of Aspergillus from different marine sources.
Marinedrugs 21 00277 g009
Marinedrugs 21 00277 g010 550
Figure 10. The proportion of Aspergillus compounds from different marine sources.
Figure 10. The proportion of Aspergillus compounds from different marine sources.
Marinedrugs 21 00277 g010
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]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

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

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop