The importance of micromonosporae in tropical, sub-tropical, terrestrial and aquatic environments
İpek Kurtböke A *A
Assoc. Prof. İpek Kurtböke has been working in the field of biodiscovery and has been an active member of the international actinomycete research community since 1982. She currently conducts research and teaches in the field of environmental and applied microbiology and biotechnology at the University of the Sunshine Coast, Queensland. She has also been an active member of the World Federation of Culture Collections (WFCC) and currently is the President of the Federation. She was also an Editorial Board member of Microbiology Australia for 20 years (2004–2024). |
Abstract
The genus Micromonospora (Ørskov 1923) is a Gram-positive, chemo-organotrophic, aerobic actinomycete, the second most predominant genus of the phylum Actinomycetota in natural environments after the genus Streptomyces, and has provided many clinically significant antibiotics, mostly aminoglycosides like gentamicin. This mini review will highlight the occurrence of this genus in diverse environments and its importance for natural product discovery and biotechnology.
Morphology and growth
The genus Micromonospora belongs to the family Micromonosporaceae and the order Micromonosporales of the class Actinomycetes and the phylum Actinomycetota. It currently has 168 species, nine subspecies and one variety (https://lpsn.dsmz.de/). Species have extensive substrate mycelium (0.2–0.6 µm diameter), and non-motile spores are borne on short hyphae of the substrate mycelium1 (Fig. 1). Spores can be spherical to oval (0.7–1.5 µm), and in most species, blunt spiny projections are formed (Fig. 2a, b). Aerial mycelium is absent, but some cultures were reported to produce sterile short hyphae upon aging.1
Single spore clusters sitting on an extensively developed substrate mycelium (©Kurtböke personal collection).
Their spores are relatively resistant to physical and chemical treatments and unaffected by high heat and desiccation.2 On growth media, they form yellow, orange, red, brown, blue-green or purple colonies, but upon sporulation the colour can turn into dark brown or black (Fig. 3).3,4 Spores can remain viable in soil, lake and marine sediments for hundreds of years, and they can tolerate reduced oxygen tensions; as a result, they can remain viable in marine sediments.2,4
Ecology
Micromonospora are chemo-organotrophic and grow in aerobic and microaerophilic conditions. They can be sensitive to lower pH and optimum growth temperature ranges between 20°C and 40°C. They are mostly mesophilic, but they have been isolated from thermal hot springs in China5 and the Mongolian desert, where temperatures can reach thermophilic conditions.6 Kurapova et al. (2008)7 reported the presence of thermotolerant Micromonospora from the desert-steppe soil samples of Mongolia and the mountainous meadow soils of the Central Caucasus. They also found the representatives of the genus Micromonospora predominating on cyanobacterial biofilms on volcanic ash near hot springs of Kamchatka.7 Micromonospora were also detected in soils of the Cisolok geothermal area in West Java, Indonesia.8 Mehetre et al. (2019)9 reported the presence of micromonosporae in the Unkeshwar hot springs of India, where the temperature of the water of the hot springs ranges between 50°C and 60°C with pH values ranging between 6.9 and 7.2. A new species named M. halotolerans growing in the presence of 5% NaCl was found in the rhizosphere of a Pisum sativum plant from Spain.10 Zenova et al. (2011)11 reported the predominance of acidophilic species of the genus Micromonospora in acidic soils such as peat, soddy podzolic and taiga podzol.
Mangroves of subtropical and tropical environments
Mangrove environments have been reported to be a prolific source for micromonosporae, including the discovery of many new species of the genus. Examples include M. avicenniae sp. nov., isolated from a root of Avicennia marina, or M. rhizosphaerae sp. nov., isolated from mangrove Excocaria agallocha rhizosphere soil of a mangrove forest in the Hainan province of China.12,13 In particular, the Southeast Asia Pacific region micromonosporae were detected in mangrove environments in countries like China, India, Indonesia, Malaysia, Thailand, Vietnam and Australia.14–20
Bioactivity of micromonosporae
Antibiotics
Starting from the early 1960s many key antibiotics were discovered from this taxon, and Micromonospora species have been prolific producers of aminoglycoside antibiotics.21,22 Key antibiotics from this genus are listed in Table 1.
| Antibiotic class | ||||
|---|---|---|---|---|
| Antibiotic/year | Producer species | References | ||
| Aminoglycosides | Gentamicin (1963) | M. purpurea (NRRL 2953) and M. echinospora (NRRL 2985) and two subspecies, M. echinospora subsp. jerruginea (NRRL 2995) and subsp. pallida (NRRL 2996). | 23 | |
| Sisomycin (1970) | M. inyoensis (NRRL 3292). | 24, 25 | ||
| Verdamicin (1975) | M. grisea (NRRL 3800). | 26 | ||
| Fortimicin (1976) | M. olivoasterospora (ATCC 21819,31010,31009). | 27 | ||
| Neomycin (1973) | Micromonospora sp. (69–683) | 28 | ||
| Sagamicin (1974) | M. sagamiensis (ATCC 21803 and ATCC 21826) | 29 | ||
| Macrolides | Megalomicins (1969) | M. megalomicea (M. megalomicea var. megalomicea (NRRL 3274) and M megalomicea var. nigra (NRRL 3275) | 30 | |
| Rosaramicin (1972) | M. rosario NRRL 3178 | 31 | ||
| Juvenimicins (1976) | M. chalcea var. izumensis (ATCC 21561) | 32 | ||
| Erythromycin B (1976) | Micromonospora sp. (1225) | 33 | ||
| Ansamysins | Halomicin (1967) | M. halophytica (NRRL 2998) and M halophytica var. nigra (NRRL 3097) | 34 | |
| Rifamycin (1975) | M ellipsospora 71372 (NRRL 8021) | 35 | ||
| Everninomicins | Everninomicin complex (1965) | M. carbonacea (NRRL 2972) and M. carbonacea var. aurantiaca (NRRL 2997) | 36 | |
| Actinomycins | Actinomycin complex (1976) | M. floridensis (NRRL 8020) | 37 | |
| Miscellaneous antibiotics | Micromonospora species | 38 | ||
Note: Table information extracted from Wagman and Weinstein (1980).38
Micromonosporae still continue to provide novel antimicrobial compounds.39 He et al. (2001)40 reported Lomaiviticins A and B, which were potent antitumor antibiotics identified from M. lomaivitiensis isolated from the inner core of an ascidian. Back et al. (2021)41 again isolated a new Micromonospora strain (28ISP2-46T), recovered from the microbiome of a mid-Atlantic deep-sea sponge. Their whole-genome sequencing revealed that the bacterium could produce a diverse array of natural products, including kosinostatin and isoquinocycline B, which exhibited both antibiotic and antitumour properties. Genomics-driven approaches are now taking the discoveries to a new frontier; examples include the identification of a benzoxazole alkaloid-encoding biosynthetic gene cluster (mich BGC) by Cheng et al. (2023)42 in a marine-derived Micromonospora sp. (SCSIO 07g95). They subsequently, via the use of heterologous expression of this BGC in Streptomyces albus, discovered five new benzoxazole alkaloids, microechmycin A–E. Kokkini et al. (2022), using the combination of LC-UV-HRMS analyses, metabolomics analysis and molecular networking (GNPS) revealed that micromonosporae in their collection produced several related spirotetronates not disclosed before, including two new phocoenamicins, phocoenamicins D and E, belonging to this class of compounds.43,44
Bioactivity from mangrove environment-associated micromonosporae has also been reported. Examples include Ismet et al. (2004)45 who isolated and chemically characterised antifungal metabolites from Micromonospora sp. (M39) isolated from mangrove rhizosphere soil. Sarveswari et al. (2020)46 reported a mangrove-derived Micromonospora sp. (RMA46) as a potential source of anti-infectives against Vibrio cholerae. Wang et al. (2019)47 identified three new isoflavonoid glycosides from the mangrove-derived M. aurantiaca (110B). Pradhan and Das (2025)48 in India, Anggelina et al. (2021)49 in Indonesia, and Lee et al. (2014)50 in Malaysia detected bioactive micromonosporae in mangrove sediments. Antimicrobial activities were also detected from Micromonospora strains isolated from Thai soils51 as well as from the stains isolated from Ninh Thuan and Binh Thuan Seas of Vietnam.52
Enzymes
Simmons et al. (2014)53 analysed meta-transcriptomes from microbial communities and, using differential expression analysis, they identified enzymes, and they noted that overexpression of these protein families in the thermophilic community resulted from expression of a small number of genes not currently represented in any protein database. Interestingly, genes in overexpressed protein families were predominantly expressed by a single actinomycete genus, which was Micromonospora. They concluded that Micromonospora dominates expression of lignocellulolytic enzymes in a thermophilic community, thus making the members of this genus a promising source of lignocellulolytic enzymes for biotechnological applications. Kumas et al. (2023)54 also agreed with Simmons et al. (2014)53 and their analysis of protein family representation in each metagenome they studied indicated that cellobiohydrolases were significantly overrepresented, and the members of the genus Micromonospora primarily housed these genes.
Amylase, lipase and urease activities were found from micromonosporae associated with mangroves in the Setiu Wetland in Terengganu in Malaysia.55 Cellulase enzymes were detected from micromonospora species and used to control plant pathogenic fungi by El-Tarabily et al. (1996).56 Again, El-Tarabily et al. (2000)57 reported production of chitinase and β-1,3-glucanase from M. carbonacea that caused extensive plasmolysis and cell wall lysis of Sclerotinia minor hyphae in vitro and in glass house tests. Termite gut-associated actinomycetes, including micromonosporae have also been reported as sources of bioactive compounds and enzymes.58
Tiong et al. (2023)59 noted that one of the exceptionally heat-resistant enzymes capable of degrading PET is the leaf-branch compost cutinase (LCC) and using molecular advances (e.g. genomic mining and in silico analysis of distant cutinase homologues), potential PET-degrading hydrolases can be obtained from actinomycetes, including from the members of Micromonospora.
Other biotechnologically important natural products
Abdelmohsen et al. (2012)60 reported antioxidant and anti-protease activities of diazepinomicin from the sponge-associated Micromonospora strain (RV115). Vitamin B12 was also reported to be produced by the members of this genus (Wagman et al. 1969).61
Conclusions
The second most predominant genus of the class Actinomycetes after the genus Streptomyces, Micromonospora will stay as one of the most important genera for biodiscovery and biotechnology,21 including the production of biofuels. Demain62 stated that one Micromonospora strain can produce 48 aminocyclitol antibiotics. The antibiotics vary in size from small molecules like cycloserine (102 Da) and bacilysin (270 Da) to polypeptides such as nisin, which contains 34 amino acid residues. With the advances in molecular techniques such as genome-based classification of micromonosporae with a focus on their biotechnological and ecological potential Carro et al. (2018)63 reported previously unrealised potential to synthesise novel specialised metabolites. They also noted that micromonosporae can adapt to key environmental variables via the distribution of key stress-related genes. Moreover, genes associated with plant interactions can open new avenues for the potential use of micromonosporae in agriculture and biotechnology.63 As stated by further investigations, such as the use of a multi-omics framework combining genome mining and metabolomics to explore the biosynthetic potential of wild-type strains of micromonosporae from extreme habitats, will reveal unknown potentials of this genus.64,65
Acknowledgements
The author thanks Professor Manfred Rohde, GBF, Germany, for his invaluable assistance with the SEM imagery (Figs 1, 2a, b).
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Assoc. Prof. İpek Kurtböke has been working in the field of biodiscovery and has been an active member of the international actinomycete research community since 1982. She currently conducts research and teaches in the field of environmental and applied microbiology and biotechnology at the University of the Sunshine Coast, Queensland. She has also been an active member of the World Federation of Culture Collections (WFCC) and currently is the President of the Federation. She was also an Editorial Board member of Microbiology Australia for 20 years (2004–2024). |
