Salinispora

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Salinispora
Cimb-44-00002-ag-Sa.png
S. arenicola strain TM223-S2
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Bacteria
Phylum: Actinomycetota
Class: Actinomycetia
Order: Micromonosporales
Family: Micromonosporaceae
Genus: Salinispora
Maldonado et al. 2005
Type species
Salinispora arenicola
Maldonado et al. 2005
Species [1]

Salinispora is a genus of obligately aerobic, gram-positive, non-acid-fast bacteria belonging to the family of Micromonosporaceae. They are heterotrophic, non-motile, and obligately grow under high osmotic/ionic-strength conditions. [2] [3] [4] They are the first identified genus of gram-positive bacteria which has a high osmotic/ionic-strength requirement for survival. [2] They are widely abundant in tropical marine sediments and were first identified in 2002. [2] This genus of bacteria has potential biotechnological significance due to their production of novel secondary metabolites which can be used pharmaceutically. [5]

Contents

There are nine known species that fall within the genus of Salinispora including the better studied S. arenicola , S. tropica , and S. pacifica. [6] [7] The clade that initially comprised only S. pacifica was further interrogated through comparative genomic analyses in 2020 to reveal six additional species. [6] The differentiation of these species is likely the result of niche differentiation rather than allopatric speciation due to the species co-occurrence. [8] Despite there being high sequence similarity among Salinispora genomes (>99% 16S rRNA sequence identity), species- and strain-based differences among biosynthetic gene clusters and products have been determined. [9] [10]

Characteristics

Salinispora members are gram-positive, filamentous bacteria which form extensively branched hyphae with smooth surfaced spores that can occur in clusters or singles. [4] During sporulation, spores may disseminate from short spore-bearing protrusions (sporophores) or directly from the base (sessile). [3] [4] They produce a range of pigments including dark brown, black, orange, and pink. [2] They likely spend a considerable amount of time in the resting stage as spores, [11] [12] with a much larger abundance and distribution of spores relative to growing individuals. They have been shown in culture to preferentially grow at the upper sediment layers where blooms at the sediment-seawater interface have been observed. [12]

Salinispora is the first identified gram-positive bacterial genus which requires a high osmotic/ionic-strength environment to survive. [2] However, it has been shown that sodium concentrations experienced in marine environments can be replaced with potassium and lithium. [13] The required ionic-strength differs among Salinispora species, but is likely due to the loss of the mscL transporter in the cell membranes in all species. [13] [14]

Species and strains within Salinispora produce a wide variety of secondary metabolites. It is likely that the biosynthetic gene clusters producing these secondary metabolites were initially acquired via horizontal gene transfer, potentially explaining the high sequence similarity among species and strains. [10] [15] The wide array of different biosynthetic gene products may have also contributed to niche differentiation. The large production of species/strains’ particular secondary metabolite lends evidence to the importance of them in bacterial survival, and can potentially be used to identify specific species and strains within the genus Salinispora. [16] [17]

Current Salinispora sampling locations Worldwide Salinispora Sample Locations.jpg
Current Salinispora sampling locations

Distribution

Salinispora are commonly found in tropical and subtropical near-shore marine sediments of the Atlantic, Pacific, and Indian oceans. [11] [18] They have been detected at depths up to 5699 m (undetermined whether actively growing or spores) and confirmed to be growing at depths up to 1100 m. [11] [12] Whether their distribution may include higher latitudes or why they are limited to equatorial regions is not yet known. Additionally, their distribution may not be limited to sediments as they have also been isolated from sponges and seaweeds.

The majority of the S. tropica isolates have been isolated in the Caribbean while the rest have been identified in all three oceans, with S. arenicola being the most geographically abundant. [19]

Pharmaceutical significance

Salinispora has been used as a model for analyzing genome sequence data in order to further uncover biosynthetic pathways among bacteria. This has been an integral part of research into using microbial natural products as leads for the discovery of traditional natural products and potential new drugs. [3] By viewing the evolutionary histories and diversity of the genus, researchers have been able to uncover mechanisms behind the strategies bacteria use to generate chemical diversity and produce diverse secondary metabolites. [3] [17] These various new secondary metabolites in Salinispora species have been identified as potentially pharmaceutically valuable. Salinispora species can be distinguished by the natural products that each species produces. [20]

Salinisporaarenicola secondary metabolites

Salinisporaarenicola secondary metabolites have a broad range of pharmaceutical applications. There are over 20 natural compounds that can be isolated from Salinispora arenicola (e.g., arenamides, arenicolides, arenimycins or salinisporamycin). The potential applications for these compounds are extensive. Over nine compounds are related to cancer cells or cancer precursor inhibition; other compounds have shown antibiotic abilities for resistant bacteria, yeast and fungi. Cycloaspeptides could be a potential treatment for asthma, as it is slightly toxic to lung fibroblasts, the human lung cells responsible for inflammation. Other compounds could be used in treatments for heavy metal poisoning or cholesterol-lowering. [20]

Salinisporapacifica secondary metabolites

Although the list of Salinisporapacifica natural compounds identified is not as extensive as found in S.arenicola, the potential pharmaceutical use of these metabolites is of great interest. Some metabolites are effective at inhibiting cancer growth. Cyanosporasides, [21] for example, were found to be a potential inhibitor of human colon carcinoma. Other metabolites can be used as antioxidants or antibiotics. [20] This species also includes some metabolites that can act as immunosuppressants. Mycalamide A was found to be a potential antiviral, antitumor and even a possible HIV treatment, as it inhibits the activation of the preferred T cell host of HIV. [22] Pacificanones A and B [23] are other metabolites with immunosuppressant capacities and possible applications in the treatment of allergies.

Lomaiviticins A and B

Salinispora pacifica produces a cytotoxic family of secondary metabolites called lomaiviticins. They were the first compounds isolated from the genus Salinispora, with the structures being published in 2001. It was initially reported that the producing bacterial strain was a new Micromonospora species with "Micromonospora lomaivitiensis" as the proposed name. Further gene sequence analysis revealed that the strain was in fact S. pacifica. [5]

Lomaiviticins are aromatic polyketides in the angucycline family and share a diazo group similar to kinamycins. [24] There are two classes of this natural product: lomaiviticin A and lomaiviticin B. Both classes demonstrate potent activity that is damaging to DNA, and is observed to be highly cytotoxic against human cancer cells. Lomaiviticin A in particular generates the greatest activity and is the most abundant of the two. [25]

Due to their unique molecular architecture and biological activities, lomaiviticins are an ideal natural product for chemical synthesis. However, notwithstanding the interest shown by the synthetic chemistry community, total synthesis of lomaiviticins has not yet been achieved and the enzymatic chemistry associated with lomaiviticin assembly has not yet been extensively researched. [26] From studying their distinctive structure, it is theorized that the synthesis of this product will lead to many novel enzymatic transformations. In addition to driving the discovery of new analogs through metabolic engineering or chemoenzymatic synthesis, further research could uncover applicable tools for biocatalysis and metabolic engineering. [24] [26]

Salinisporatropica secondary metabolites

The number of secondary metabolites identified and isolated from Salinispora tropica is fewer than the two other species. However, the pharmaceutical and clinical relevance of these metabolites is much higher. As of yet Salinosporamide is the most successful secondary metabolite of Salinisopora from the clinical point of view. It has already been moved into human trials, and it has shown to be a strong anti-cancer agent. [27] Salinispora tropica also produces antiprotealide, another anti-cancer agent which is potentially the strongest cancer inhibitor within the Salinospora secondary metabolite lists. This natural compound is a very potent cytotoxin for myeloma cells. [28]

Related Research Articles

<i>Streptomyces</i> Genus of bacteria

Streptomyces is the largest genus of Actinomycetota, and the type genus of the family Streptomycetaceae. Over 700 species of Streptomyces bacteria have been described. As with the other Actinomycetota, streptomycetes are gram-positive, and have very large genomes with high GC content. Found predominantly in soil and decaying vegetation, most streptomycetes produce spores, and are noted for their distinct "earthy" odor that results from production of a volatile metabolite, geosmin. Different strains of the same species may colonize very diverse environments.

<span class="mw-page-title-main">Natural product</span> Chemical compound or substance produced by a living organism, found in nature

A natural product is a natural compound or substance produced by a living organism—that is, found in nature. In the broadest sense, natural products include any substance produced by life. Natural products can also be prepared by chemical synthesis and have played a central role in the development of the field of organic chemistry by providing challenging synthetic targets. The term natural product has also been extended for commercial purposes to refer to cosmetics, dietary supplements, and foods produced from natural sources without added artificial ingredients.

<i>Burkholderia</i> Genus of bacteria

Burkholderia is a genus of Pseudomonadota whose pathogenic members include the Burkholderia cepacia complex, which attacks humans and Burkholderia mallei, responsible for glanders, a disease that occurs mostly in horses and related animals; Burkholderia pseudomallei, causative agent of melioidosis; and Burkholderia cepacia, an important pathogen of pulmonary infections in people with cystic fibrosis (CF). Burkholderia species is also found in marine environments. S.I. Paul et al. (2021) isolated and characterized Burkholderia cepacia from marine sponges of the Saint Martin's Island of the Bay of Bengal, Bangladesh.

<span class="mw-page-title-main">Gammaproteobacteria</span> Class of bacteria

Gammaproteobacteria is a class of bacteria in the phylum Pseudomonadota. It contains about 250 genera, which makes it the most genus-rich taxon of the Prokaryotes. Several medically, ecologically, and scientifically important groups of bacteria belong to this class. It is composed by all Gram-negative microbes and is the most phylogenetically and physiologically diverse class of Proteobacteria.

<span class="mw-page-title-main">Salinosporamide A</span> Chemical compound

Salinosporamide A (Marizomib) is a potent proteasome inhibitor being studied as a potential anticancer agent. It entered phase I human clinical trials for the treatment of multiple myeloma, only three years after its discovery in 2003. This marine natural product is produced by the obligate marine bacteria Salinispora tropica and Salinispora arenicola, which are found in ocean sediment. Salinosporamide A belongs to a family of compounds, known collectively as salinosporamides, which possess a densely functionalized γ-lactam-β-lactone bicyclic core.

<span class="mw-page-title-main">Nereus Pharmaceuticals</span>

Nereus Pharmaceuticals was a pharmaceutical company focused on the development of natural products from marine microbial and other natural sources into small molecule human therapeutics. The major disease area addressed by Nereus is cancer. Nereus was purchased by Triphase Research and Development in 2012.

<i>Streptomyces griseus</i> Species of bacterium

Streptomyces griseus is a species of bacteria in the genus Streptomyces commonly found in soil. A few strains have been also reported from deep-sea sediments. It is a Gram-positive bacterium with high GC content. Along with most other streptomycetes, S. griseus strains are well known producers of antibiotics and other such commercially significant secondary metabolites. These strains are known to be producers of 32 different structural types of bioactive compounds. Streptomycin, the first antibiotic ever reported from a bacterium, comes from strains of S. griseus. Recently, the whole genome sequence of one of its strains had been completed.

<span class="mw-page-title-main">Sporolides</span> Chemical compound

Sporolides A and B are polycyclic macrolides extracted from the obligate marine bacterium Salinispora tropica, which is found in ocean sediment. They are composed of a chlorinated cyclopenta[a]indene ring and a cyclohexenone moiety. They were the second group of compounds isolated from Salinispora, and were said to indicate the potential of marine actinomycetes as a source of novel secondary metabolites. The structures and absolute stereochemistries of both metabolites were elucidated using a combination of NMR spectroscopy and X-ray crystallography.

The salinosporamides are a group of closely related chemical compounds isolated from marine bacteria in the genus Salinispora. They possess a densely functionalized γ-lactam-β-lactone bicyclic core.

Salinispora arenicola is an obligate marine actinomycete bacterium species. It produces salinosporamide, a potential anti-cancer agent.

Salinispora tropica is an obligate marine actinomycete bacterium species. It produces salinosporamide A and salinosporamide B, potential anti-cancer agents, as well as the polycyclic macrolides sporolide A and B.

<span class="mw-page-title-main">Marinone</span> Chemical compound

Marinone is an antibiotic made by marine actinomycetes.

<span class="mw-page-title-main">Stevensine</span> Bio-active alkaloid isolated from a marine sponge

Stevensine is a bromopyrrole alkaloid originally isolated from an unidentified Micronesian marine sponge, as well as a New Caledonian sponge, Pseudaxinyssa cantharella and Axinella corrugata. Total synthesis of stevensine has been achieved by Ying-zi Xu et al., and investigations into the biosynthetic origin has been explored by Paul Andrade et al. Understanding methods to synthesize stevensine and other similar compounds is an important step to accomplish, as marine sponges contain numerous biologically active metabolites that have been shown to function as anything from antitumor to antibacterial agents when tested for medicinal applications. Reasons for why marine sponges contain so many bio-active chemicals has been attributed to their sessile nature, and the need to produce chemical defenses to ensure survival. However, since many of these compounds naturally occur in small amounts, harvesting the sponges has in the past led to near-extinction of some species.

<span class="mw-page-title-main">Lactocillin</span> Chemical compound

Lactocillin is a thiopeptide antibiotic which is encoded for and produced by biosynthetic genes clusters in the bacteria Lactobacillus gasseri. Lactocillin was discovered and purified in 2014. Lactobacillus gasseri is one of the four Lactobacillus bacteria found to be most common in the human vaginal microbiome. Due to increasing levels of pathogenic resistance to known antibiotics, novel antibiotics are increasingly valuable. Lactocillin could function as a new antibiotic that could help people fight off infections that are resistant to many other antibiotics.

Salinispora pacifica is an obligate marine actinomycetes bacterium species in the genus Salinispora.

Plesiocystis pacifica is a species of marine myxobacteria. Like other members of this order, P. pacifica is a rod-shaped Gram-negative bacterium that can move by gliding and can form aggregates of cells called fruiting bodies. The species was first described in 2003, based on two strains isolated from samples collected from the Pacific coast of Japan.

Enhygromyxa salina is a species of marine myxobacteria. Like other members of this order, E. salina is a rod-shaped Gram-negative bacterium that can move by gliding and can form aggregates of cells called fruiting bodies. E. salina is slightly halophilic (salt-tolerant) and can grow at lower temperatures than other marine myxobacteria. Several novel secondary metabolites have been identified in the species, including unusual sterols. The species was first described in 2003, based on six strains isolated from samples collected from the coastlines of Japan.

<span class="mw-page-title-main">Undecylprodigiosin</span> Chemical compound

Undecylprodigiosin is an alkaloid produced by some Actinomycetes bacteria. It is a member of the prodiginines group of natural products and has been investigated for potential antimalarial activity.

<span class="mw-page-title-main">Prodiginines</span>

The prodiginines are a family of red tripyrrole dyestuffs produced by Gammaproteobacteria as well as some Actinomycetota. The group is named after prodigiosin (prodiginine) and is biosynthesized through a common set of enzymes. They are interesting due to their history and their varied biological activity.

<span class="mw-page-title-main">Enterocin</span> Chemical compound

Enterocin and its derivatives are bacteriocins synthesized by the lactic acid bacteria, Enterococcus. This class of polyketide antibiotics are effective against foodborne pathogens including L. monocytogenes, Listeria, and Bacillus. Due to its proteolytic degradability in the gastrointestinal tract, enterocin is used for controlling foodborne pathogens via human consumption.

References

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  14. ↑ Bucarey SA, Penn K, Paul L, Fenical W, Jensen PR (June 2012). "Genetic complementation of the obligate marine actinobacterium Salinispora tropica with the large mechanosensitive channel gene mscL rescues cells from osmotic downshock". Applied and Environmental Microbiology. 78 (12): 4175–4182. Bibcode:2012ApEnM..78.4175B. doi:10.1128/aem.00577-12. PMC   3370544 . PMID   22492446.
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  19. ↑ Freel KC, Edlund A, Jensen PR (February 2012). "Microdiversity and evidence for high dispersal rates in the marine actinomycete 'Salinispora pacifica'". Environmental Microbiology. 14 (2): 480–493. doi:10.1111/j.1462-2920.2011.02641.x. PMC   3272088 . PMID   22117917.
  20. 1 2 3 Kim H, Kim S, Kim M, Lee C, Yang I, Nam SJ (December 2020). "Bioactive natural products from the genus Salinospora: a review". Archives of Pharmacal Research. 43 (12): 1230–1258. doi:10.1007/s12272-020-01288-1. PMID   33237436. S2CID   227166135.
  21. ↑ Kersten RD, Lane AL, Nett M, Richter TK, Duggan BM, Dorrestein PC, Moore BS (May 2013). "Bioactivity-guided genome mining reveals the lomaiviticin biosynthetic gene cluster in Salinispora tropica". ChemBioChem. 14 (8): 955–962. doi:10.1002/cbic.201300147. PMC   3755882 . PMID   23649992.
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  26. 1 2 Achanta S (2009). Studies toward the synthesis of lomaiviticins A and B and englerin A (Ph.D. thesis). Saint Louis, Mo: Washington University. OCLC   671642940.
  27. ↑ Chauhan D, Catley L, Li G, Podar K, Hideshima T, Velankar M, et al. (November 2005). "A novel orally active proteasome inhibitor induces apoptosis in multiple myeloma cells with mechanisms distinct from Bortezomib". Cancer Cell. 8 (5): 407–419. doi: 10.1016/j.ccr.2005.10.013 . PMID   16286248.
  28. ↑ Manam RR, Macherla VR, Tsueng G, Dring CW, Weiss J, Neuteboom ST, et al. (February 2009). "Antiprotealide is a natural product". Journal of Natural Products. 72 (2): 295–297. doi:10.1021/np800578e. PMID   19133779.
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