Marie-Katherin Zühlke, Elizabeth Ficko-Blean, Daniel Bartosik, Nicolas Terrapon, Alexandra Jeudy, Murielle Jam, Fengqing Wang, Norma Welsch, Alexandra Dürwald, Laura Torres Martin, Robert Larocque, Diane Jouanneau, Tom Eisenack, François Thomas, Anke Trautwein-Schult, Hanno Teeling, Dörte Becher, Thomas Schweder, Mirjam Czjzek
{"title":"揭示新型碳水化合物结合模块在浮游植物大量繁殖期间海洋类杆菌多模块蛋白与层叠蛋白相互作用中的作用","authors":"Marie-Katherin Zühlke, Elizabeth Ficko-Blean, Daniel Bartosik, Nicolas Terrapon, Alexandra Jeudy, Murielle Jam, Fengqing Wang, Norma Welsch, Alexandra Dürwald, Laura Torres Martin, Robert Larocque, Diane Jouanneau, Tom Eisenack, François Thomas, Anke Trautwein-Schult, Hanno Teeling, Dörte Becher, Thomas Schweder, Mirjam Czjzek","doi":"10.1111/1462-2920.16624","DOIUrl":null,"url":null,"abstract":"<p>Laminarin, a β(1,3)-glucan, serves as a storage polysaccharide in marine microalgae such as diatoms. Its abundance, water solubility and simple structure make it an appealing substrate for marine bacteria. Consequently, many marine bacteria have evolved strategies to scavenge and decompose laminarin, employing carbohydrate-binding modules (CBMs) as crucial components. In this study, we characterized two previously unassigned domains as laminarin-binding CBMs in multimodular proteins from the marine bacterium <i>Christiangramia forsetii</i> KT0803<sup>T</sup>, thereby introducing the new laminarin-binding CBM families CBM102 and CBM103. We identified four CBM102s in a surface glycan-binding protein (SGBP) and a single CBM103 linked to a glycoside hydrolase module from family 16 (GH16_3). Our analysis revealed that both modular proteins have an elongated shape, with GH16_3 exhibiting greater flexibility than SGBP. This flexibility may aid in the recognition and/or degradation of laminarin, while the constraints in SGBP could facilitate the docking of laminarin onto the bacterial surface. Exploration of bacterial metagenome-assembled genomes (MAGs) from phytoplankton blooms in the North Sea showed that both laminarin-binding CBM families are widespread among marine <i>Bacteroidota</i>. The high protein abundance of CBM102- and CBM103-containing proteins during phytoplankton blooms further emphasizes their significance in marine laminarin utilization.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":null,"pages":null},"PeriodicalIF":4.3000,"publicationDate":"2024-05-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16624","citationCount":"0","resultStr":"{\"title\":\"Unveiling the role of novel carbohydrate-binding modules in laminarin interaction of multimodular proteins from marine Bacteroidota during phytoplankton blooms\",\"authors\":\"Marie-Katherin Zühlke, Elizabeth Ficko-Blean, Daniel Bartosik, Nicolas Terrapon, Alexandra Jeudy, Murielle Jam, Fengqing Wang, Norma Welsch, Alexandra Dürwald, Laura Torres Martin, Robert Larocque, Diane Jouanneau, Tom Eisenack, François Thomas, Anke Trautwein-Schult, Hanno Teeling, Dörte Becher, Thomas Schweder, Mirjam Czjzek\",\"doi\":\"10.1111/1462-2920.16624\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p>Laminarin, a β(1,3)-glucan, serves as a storage polysaccharide in marine microalgae such as diatoms. Its abundance, water solubility and simple structure make it an appealing substrate for marine bacteria. Consequently, many marine bacteria have evolved strategies to scavenge and decompose laminarin, employing carbohydrate-binding modules (CBMs) as crucial components. In this study, we characterized two previously unassigned domains as laminarin-binding CBMs in multimodular proteins from the marine bacterium <i>Christiangramia forsetii</i> KT0803<sup>T</sup>, thereby introducing the new laminarin-binding CBM families CBM102 and CBM103. We identified four CBM102s in a surface glycan-binding protein (SGBP) and a single CBM103 linked to a glycoside hydrolase module from family 16 (GH16_3). Our analysis revealed that both modular proteins have an elongated shape, with GH16_3 exhibiting greater flexibility than SGBP. This flexibility may aid in the recognition and/or degradation of laminarin, while the constraints in SGBP could facilitate the docking of laminarin onto the bacterial surface. Exploration of bacterial metagenome-assembled genomes (MAGs) from phytoplankton blooms in the North Sea showed that both laminarin-binding CBM families are widespread among marine <i>Bacteroidota</i>. The high protein abundance of CBM102- and CBM103-containing proteins during phytoplankton blooms further emphasizes their significance in marine laminarin utilization.</p>\",\"PeriodicalId\":11898,\"journal\":{\"name\":\"Environmental microbiology\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":4.3000,\"publicationDate\":\"2024-05-16\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16624\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Environmental microbiology\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://onlinelibrary.wiley.com/doi/10.1111/1462-2920.16624\",\"RegionNum\":2,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q2\",\"JCRName\":\"MICROBIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Environmental microbiology","FirstCategoryId":"99","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/1462-2920.16624","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
Unveiling the role of novel carbohydrate-binding modules in laminarin interaction of multimodular proteins from marine Bacteroidota during phytoplankton blooms
Laminarin, a β(1,3)-glucan, serves as a storage polysaccharide in marine microalgae such as diatoms. Its abundance, water solubility and simple structure make it an appealing substrate for marine bacteria. Consequently, many marine bacteria have evolved strategies to scavenge and decompose laminarin, employing carbohydrate-binding modules (CBMs) as crucial components. In this study, we characterized two previously unassigned domains as laminarin-binding CBMs in multimodular proteins from the marine bacterium Christiangramia forsetii KT0803T, thereby introducing the new laminarin-binding CBM families CBM102 and CBM103. We identified four CBM102s in a surface glycan-binding protein (SGBP) and a single CBM103 linked to a glycoside hydrolase module from family 16 (GH16_3). Our analysis revealed that both modular proteins have an elongated shape, with GH16_3 exhibiting greater flexibility than SGBP. This flexibility may aid in the recognition and/or degradation of laminarin, while the constraints in SGBP could facilitate the docking of laminarin onto the bacterial surface. Exploration of bacterial metagenome-assembled genomes (MAGs) from phytoplankton blooms in the North Sea showed that both laminarin-binding CBM families are widespread among marine Bacteroidota. The high protein abundance of CBM102- and CBM103-containing proteins during phytoplankton blooms further emphasizes their significance in marine laminarin utilization.
期刊介绍:
Environmental Microbiology provides a high profile vehicle for publication of the most innovative, original and rigorous research in the field. The scope of the Journal encompasses the diversity of current research on microbial processes in the environment, microbial communities, interactions and evolution and includes, but is not limited to, the following:
the structure, activities and communal behaviour of microbial communities
microbial community genetics and evolutionary processes
microbial symbioses, microbial interactions and interactions with plants, animals and abiotic factors
microbes in the tree of life, microbial diversification and evolution
population biology and clonal structure
microbial metabolic and structural diversity
microbial physiology, growth and survival
microbes and surfaces, adhesion and biofouling
responses to environmental signals and stress factors
modelling and theory development
pollution microbiology
extremophiles and life in extreme and unusual little-explored habitats
element cycles and biogeochemical processes, primary and secondary production
microbes in a changing world, microbially-influenced global changes
evolution and diversity of archaeal and bacterial viruses
new technological developments in microbial ecology and evolution, in particular for the study of activities of microbial communities, non-culturable microorganisms and emerging pathogens