Laurence Meunier, Rodrigo Costa, Tina Keller-Costa, David Cannella, Etienne Dechamps, Isabelle F George
{"title":"通过选择高效降解几丁质的海洋细菌群,发现了新的潜在几丁质降解者。","authors":"Laurence Meunier, Rodrigo Costa, Tina Keller-Costa, David Cannella, Etienne Dechamps, Isabelle F George","doi":"10.1128/spectrum.00886-24","DOIUrl":null,"url":null,"abstract":"<p><p>Chitin degradation is a keystone process in the oceans, mediated by marine microorganisms with the help of several enzymes, mostly chitinases. Sediment, seawater, and filter-feeding marine invertebrates, such as sponges, are known to harbor chitin-degrading bacteria and are presumably hotspots for chitin turnover. Here, we employed an artificial selection process involving enrichment cultures derived from microbial communities associated with the marine sponge <i>Hymeniacidon perlevis</i>, its surrounding seawater and sediment, to select bacterial consortia capable of degrading raw chitin. Throughout the artificial selection process, chitin degradation rates and the taxonomic composition of the four successive enrichment cultures were followed. To the best of our knowledge, chitin degradation was characterized for the first time using size exclusion chromatography, which revealed significant shifts in the numbered average chitin molecular weight, strongly suggesting the involvement of endo-chitinases in the breakdown of the chitin polymer during the enrichment process. Concomitantly with chitin degradation, the enrichment cultures exhibited a decrease in alpha diversity compared with the environmental samples. Notably, some of the dominant taxa in the enriched communities, such as <i>Motilimonas</i>, <i>Arcobacter</i>, and <i>Halarcobacter</i>, were previously unknown to be involved in chitin degradation. In particular, the analysis of published genomes of these genera suggests a pivotal role of <i>Motilimonas</i> in the hydrolytic cleavage of chitin. This study provides context to the microbiome of the marine sponge <i>Hymeniacidon perlevis</i> in light of its environmental surroundings and opens new ground to the future discovery and characterization of novel enzymes of marine origin involved in chitin degradation processes.IMPORTANCEChitin is the second most abundant biopolymer on Earth after cellulose, and the most abundant in the marine environment. At present, industrial processes for the conversion of seafood waste into chitin, chitosan, and chitooligosaccharide (COS) rely on the use of high amounts of concentrated acids or strong alkali at high temperature. Developing bio-based methods to transform available chitin into valuable compounds, such as chitosan and COS, holds promise in promoting a more sustainable, circular bioeconomy. By employing an artificial selection procedure based on chitin as a sole C and N source, we discovered microorganisms so-far unknown to metabolize chitin in the rare microbial biosphere of several marine biotopes. This finding represents a first important step on the path towards characterizing and exploiting potentially novel enzymes of marine origin with biotechnological interest, since products of chitin degradation may find applications across several sectors, such as agriculture, pharmacy, and waste management.</p>","PeriodicalId":18670,"journal":{"name":"Microbiology spectrum","volume":null,"pages":null},"PeriodicalIF":3.7000,"publicationDate":"2024-11-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11537107/pdf/","citationCount":"0","resultStr":"{\"title\":\"Selection of marine bacterial consortia efficient at degrading chitin leads to the discovery of new potential chitin degraders.\",\"authors\":\"Laurence Meunier, Rodrigo Costa, Tina Keller-Costa, David Cannella, Etienne Dechamps, Isabelle F George\",\"doi\":\"10.1128/spectrum.00886-24\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Chitin degradation is a keystone process in the oceans, mediated by marine microorganisms with the help of several enzymes, mostly chitinases. Sediment, seawater, and filter-feeding marine invertebrates, such as sponges, are known to harbor chitin-degrading bacteria and are presumably hotspots for chitin turnover. Here, we employed an artificial selection process involving enrichment cultures derived from microbial communities associated with the marine sponge <i>Hymeniacidon perlevis</i>, its surrounding seawater and sediment, to select bacterial consortia capable of degrading raw chitin. Throughout the artificial selection process, chitin degradation rates and the taxonomic composition of the four successive enrichment cultures were followed. To the best of our knowledge, chitin degradation was characterized for the first time using size exclusion chromatography, which revealed significant shifts in the numbered average chitin molecular weight, strongly suggesting the involvement of endo-chitinases in the breakdown of the chitin polymer during the enrichment process. Concomitantly with chitin degradation, the enrichment cultures exhibited a decrease in alpha diversity compared with the environmental samples. Notably, some of the dominant taxa in the enriched communities, such as <i>Motilimonas</i>, <i>Arcobacter</i>, and <i>Halarcobacter</i>, were previously unknown to be involved in chitin degradation. In particular, the analysis of published genomes of these genera suggests a pivotal role of <i>Motilimonas</i> in the hydrolytic cleavage of chitin. This study provides context to the microbiome of the marine sponge <i>Hymeniacidon perlevis</i> in light of its environmental surroundings and opens new ground to the future discovery and characterization of novel enzymes of marine origin involved in chitin degradation processes.IMPORTANCEChitin is the second most abundant biopolymer on Earth after cellulose, and the most abundant in the marine environment. At present, industrial processes for the conversion of seafood waste into chitin, chitosan, and chitooligosaccharide (COS) rely on the use of high amounts of concentrated acids or strong alkali at high temperature. Developing bio-based methods to transform available chitin into valuable compounds, such as chitosan and COS, holds promise in promoting a more sustainable, circular bioeconomy. By employing an artificial selection procedure based on chitin as a sole C and N source, we discovered microorganisms so-far unknown to metabolize chitin in the rare microbial biosphere of several marine biotopes. 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Selection of marine bacterial consortia efficient at degrading chitin leads to the discovery of new potential chitin degraders.
Chitin degradation is a keystone process in the oceans, mediated by marine microorganisms with the help of several enzymes, mostly chitinases. Sediment, seawater, and filter-feeding marine invertebrates, such as sponges, are known to harbor chitin-degrading bacteria and are presumably hotspots for chitin turnover. Here, we employed an artificial selection process involving enrichment cultures derived from microbial communities associated with the marine sponge Hymeniacidon perlevis, its surrounding seawater and sediment, to select bacterial consortia capable of degrading raw chitin. Throughout the artificial selection process, chitin degradation rates and the taxonomic composition of the four successive enrichment cultures were followed. To the best of our knowledge, chitin degradation was characterized for the first time using size exclusion chromatography, which revealed significant shifts in the numbered average chitin molecular weight, strongly suggesting the involvement of endo-chitinases in the breakdown of the chitin polymer during the enrichment process. Concomitantly with chitin degradation, the enrichment cultures exhibited a decrease in alpha diversity compared with the environmental samples. Notably, some of the dominant taxa in the enriched communities, such as Motilimonas, Arcobacter, and Halarcobacter, were previously unknown to be involved in chitin degradation. In particular, the analysis of published genomes of these genera suggests a pivotal role of Motilimonas in the hydrolytic cleavage of chitin. This study provides context to the microbiome of the marine sponge Hymeniacidon perlevis in light of its environmental surroundings and opens new ground to the future discovery and characterization of novel enzymes of marine origin involved in chitin degradation processes.IMPORTANCEChitin is the second most abundant biopolymer on Earth after cellulose, and the most abundant in the marine environment. At present, industrial processes for the conversion of seafood waste into chitin, chitosan, and chitooligosaccharide (COS) rely on the use of high amounts of concentrated acids or strong alkali at high temperature. Developing bio-based methods to transform available chitin into valuable compounds, such as chitosan and COS, holds promise in promoting a more sustainable, circular bioeconomy. By employing an artificial selection procedure based on chitin as a sole C and N source, we discovered microorganisms so-far unknown to metabolize chitin in the rare microbial biosphere of several marine biotopes. This finding represents a first important step on the path towards characterizing and exploiting potentially novel enzymes of marine origin with biotechnological interest, since products of chitin degradation may find applications across several sectors, such as agriculture, pharmacy, and waste management.
期刊介绍:
Microbiology Spectrum publishes commissioned review articles on topics in microbiology representing ten content areas: Archaea; Food Microbiology; Bacterial Genetics, Cell Biology, and Physiology; Clinical Microbiology; Environmental Microbiology and Ecology; Eukaryotic Microbes; Genomics, Computational, and Synthetic Microbiology; Immunology; Pathogenesis; and Virology. Reviews are interrelated, with each review linking to other related content. A large board of Microbiology Spectrum editors aids in the development of topics for potential reviews and in the identification of an editor, or editors, who shepherd each collection.