Biological Potential of Chitinolytic Marine Bacteria

Paulsen, Sara Skøtt; Andersen, Birgitte; Gram, Lone; Machado, Henrique

doi:10.3390/md14120230

Cited by 39 publications

(28 citation statements)

References 59 publications

(66 reference statements)

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“…JC28, many P. piscicida strains have also shown strong inhibition against vibrios and other bacterial pathogens (39,40) and antifungal activity against several fungi, including Arthrinium c.f. saccharicola (41) and Fusarium oxysporum (42). P. piscicida strains have also demonstrated eukaryotic toxicity, killing Artemia nauplii brine shrimp and Caenorhabditis elegans nematodes (43), and lysing Gymnodinium catenatum algal cells (44).…”

Section: Discussionmentioning

confidence: 99%

Hawaiian Bobtail Squid Symbionts Inhibit Marine Bacteria via Production of Specialized Metabolites, Including New Bromoalterochromides BAC-D/D′

Suria

Tan

Kerwin

et al. 2020

mSphere

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ABSTRACT The Hawaiian bobtail squid, Euprymna scolopes, has a symbiotic bacterial consortium in the accessory nidamental gland (ANG), a female reproductive organ that protects eggs against fouling microorganisms. To test the antibacterial activity of ANG community members, 19 bacterial isolates were screened for their ability to inhibit Gram-negative and Gram-positive bacteria, of which two strains were inhibitory. These two antibacterial isolates, Leisingera sp. ANG59 and Pseudoalteromonas sp. JC28, were subjected to further genomic characterization. Genomic analysis of Leisingera sp. ANG59 revealed a biosynthetic gene cluster encoding the antimicrobial compound indigoidine. The genome of Pseudoalteromonas sp. JC28 had a 14-gene cluster with >95% amino acid identity to a known bromoalterochromide (BAC) cluster. Chemical analysis confirmed production of known BACs, BAC-A/A′ (compounds 1a/1b), as well as two new derivatives, BAC-D/D′ (compounds 2a/2b). Extensive nuclear magnetic resonance (NMR) analyses allowed complete structural elucidation of compounds 2a/2b, and the absolute stereochemistry was unambiguously determined using an optimized Marfey’s method. The BACs were then investigated for in vitro antibacterial, antifungal, and nitric oxide (NO) inhibitory activity. Compounds 1a/1b were active against the marine bacteria Bacillus algicola and Vibrio fischeri, while compounds 2a/2b were active only against B. algicola. Compounds 1a/1b inhibited NO production via lipopolysaccharide (LPS)-induced inflammation in RAW264.7 macrophage cells and also inhibited the pathogenic fungus Fusarium keratoplasticum, which, coupled with their antibacterial activity, suggests that these polyketide-nonribosomal peptides may be used for squid egg defense against potential pathogens and/or fouling microorganisms. These results indicate that BACs may provide Pseudoalteromonas sp. JC28 an ecological niche, facilitating competition against nonsymbiotic microorganisms in the host’s environment. IMPORTANCE Animals that deposit eggs must protect their embryos from fouling and disease by microorganisms to ensure successful development. Although beneficial bacteria are hypothesized to contribute to egg defense in many organisms, the mechanisms of this protection are only recently being elucidated. Our previous studies of the Hawaiian bobtail squid focused on fungal inhibition by beneficial bacterial symbionts of a female reproductive gland and eggs. Herein, using genomic and chemical analyses, we demonstrate that symbiotic bacteria from this gland can also inhibit other marine bacteria in vitro. One bacterial strain in particular, Pseudoalteromonas sp. JC28, had broad-spectrum abilities to inhibit potential fouling bacteria, in part via production of novel bromoalterochromide metabolites, confirmed via genomic annotation of the associated biosynthetic gene cluster. Our results suggest that these bacterial metabolites may contribute to antimicrobial activity in this association and that such defensive symbioses are underutilized sources for discovering novel antimicrobial compounds.

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Section: Discussionmentioning

confidence: 99%

Hawaiian Bobtail Squid Symbionts Inhibit Marine Bacteria via Production of Specialized Metabolites, Including New Bromoalterochromides BAC-D/D′

Suria

Tan

Kerwin

et al. 2020

mSphere

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“…In bacteria, the majority of chitinases belong to glycosyl hydrolase (GH) family 18 (25). Recently, chitinases belonging to GH family 19 have been discovered in a few groups of prokaryotes (26–30), and we have found that the genomes of 10 marine chitinolytic bacteria, including Pseudoalteromonas , all contain at least one GH19 chitinase (31).…”

Section: Introductionmentioning

confidence: 92%

Marine Chitinolytic Pseudoalteromonas Represents an Untapped Reservoir of Bioactive Potential

et al. 2019

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Chitin is the most abundant polymer in the marine environment and a nutrient-rich surface for adhering marine bacteria. We have previously shown that chitin can induce the production of antibiotic compounds in Vibrionaceae, suggesting that the discovery of novel bioactive molecules from bacteria can be facilitated by mimicking their natural habitat. The purpose of this study was to determine the glycosyl hydrolase (GH) profiles of strains of the genus Pseudoalteromonas to enable selection of presumed growth substrates and explore possible links to secondary metabolism. Genomic analyses were conducted on 62 pigmented and 95 nonpigmented strains. Analysis of the total GH profiles and multidimensional scaling suggested that the degradation of chitin is a significant trait of pigmented strains, whereas nonpigmented strains seem to be driven toward the degradation of alga-derived carbohydrates. The genomes of all pigmented strains and 40 nonpigmented strains encoded at least one conserved chitin degradation cluster, and chitinolytic activity was phenotypically confirmed. Additionally, the genomes of all pigmented and a few nonpigmented strains encoded chitinases of the rare GH family 19. Pigmented strains devote up to 15% of their genome to secondary metabolism, while for nonpigmented species it was 3% at most. Thus, pigmented Pseudoalteromonas strains have a bioactive potential similar to that of well-known antibiotic producers of the Actinobacteria phylum. Growth on chitin did not measurably enhance the antibacterial activity of the strains; however, we demonstrated a remarkable co-occurrence of chitin degradation and the potential for secondary metabolite production in pigmented Pseudoalteromonas strains. This indicates that chitin and its colonizers of the Pseudoalteromonas genus represent a so far underexplored niche for novel enzymes and bioactive compounds. IMPORTANCE Infectious bacteria are developing and spreading resistance to conventional treatments at a rapid pace. To provide novel potent antimicrobials, we must develop new bioprospecting strategies. Here, we combined in silico and phenotypic approaches to explore the bioactive potential of the marine bacterial genus Pseudoalteromonas. We found that pigmented strains in particular represent an untapped resource of secondary metabolites and that they also harbor an elaborate chitinolytic machinery. Furthermore, our analysis showed that chitin is likely a preferred substrate for pigmented species, in contrast to nonpigmented species. Potentially, chitin could facilitate the production of new secondary metabolites in pigmented Pseudoalteromonas strains.

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“…Although the chitinolytic activity of some species has been reported in the literature, it remains unknown which group of microorganisms is the most effective at decomposing this polymer. Several authors have reported marine ecosystems as a main source of chitinase-producing microorganisms, mainly bacteria (Sara et al, 2016; Swiontek et al, 2014; Suresh, 2012). Chitinolytic bacteria represent only 4% of the currently known bacteria (Swiontek et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Isolation and identification of marine strains ofStenotrophomona maltophiliawith high chitinolytic activity

Salas-Ovilla¹,

Gálvez-López²,

Vázquez-Ovando³

et al. 2019

PeerJ

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Chitin is the second most abundant organic compound in nature and represents a rich carbon and nitrogen source that is primarily transformed by bacterial communities. Bacteria capable of gradually hydrolyzing chitin into N-acetylglucosamine monomers can have applications in the transformation of residues from shrimp and other crustaceans. The objective of the present study was to isolate, characterize and identify microorganisms with high chitinolytic activity. These microorganisms were isolated and characterized based on macro- and microscopic morphological traits. Strains were selected on colloidal chitin agar medium primarily based on a hydrolysis halo larger than 2 mm and a growing phase no longer than 6 days. Secondary selection consisted of semi-quantitative evaluation of chitinolytic activity with a drop dilution assay. From the above, ten strains were selected. Then, strain-specific activity was evaluated. The B4 strain showed the highest specific activity, which was 6,677.07 U/mg protein. Molecular identification indicated that the isolated strains belong to the species Stenotrophomonas maltophilia.

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Biological Potential of Chitinolytic Marine Bacteria

Cited by 39 publications

References 59 publications

Hawaiian Bobtail Squid Symbionts Inhibit Marine Bacteria via Production of Specialized Metabolites, Including New Bromoalterochromides BAC-D/D′

Hawaiian Bobtail Squid Symbionts Inhibit Marine Bacteria via Production of Specialized Metabolites, Including New Bromoalterochromides BAC-D/D′

Marine Chitinolytic Pseudoalteromonas Represents an Untapped Reservoir of Bioactive Potential

Isolation and identification of marine strains ofStenotrophomona maltophiliawith high chitinolytic activity

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