Genomic and transcriptomic landscapes and evolutionary dynamics of molluscan glycoside hydrolase families with implications for algae-feeding biology
The hydrolysis of sugar-containing compounds by glycoside hydrolases (GHs) plays essential roles in many major biological processes, but to date our systematic understanding of the functional diversity and evolution of GH families remains largely limited to a few well-studied terrestrial animals. Mo...
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Elsevier
2020-01-01
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Series: | Computational and Structural Biotechnology Journal |
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Online Access: | http://www.sciencedirect.com/science/article/pii/S2001037020304050 |
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record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Jing Wang Hongwei Yu Lijie Yao Yuli Li Fuyun Liu Wentao Han Cong Cui Jingjie Hu Zhenmin Bao Shi Wang |
spellingShingle |
Jing Wang Hongwei Yu Lijie Yao Yuli Li Fuyun Liu Wentao Han Cong Cui Jingjie Hu Zhenmin Bao Shi Wang Genomic and transcriptomic landscapes and evolutionary dynamics of molluscan glycoside hydrolase families with implications for algae-feeding biology Computational and Structural Biotechnology Journal Mollusc Glycoside hydrolase Gene family expansion Adaptive evolution Algae feeding |
author_facet |
Jing Wang Hongwei Yu Lijie Yao Yuli Li Fuyun Liu Wentao Han Cong Cui Jingjie Hu Zhenmin Bao Shi Wang |
author_sort |
Jing Wang |
title |
Genomic and transcriptomic landscapes and evolutionary dynamics of molluscan glycoside hydrolase families with implications for algae-feeding biology |
title_short |
Genomic and transcriptomic landscapes and evolutionary dynamics of molluscan glycoside hydrolase families with implications for algae-feeding biology |
title_full |
Genomic and transcriptomic landscapes and evolutionary dynamics of molluscan glycoside hydrolase families with implications for algae-feeding biology |
title_fullStr |
Genomic and transcriptomic landscapes and evolutionary dynamics of molluscan glycoside hydrolase families with implications for algae-feeding biology |
title_full_unstemmed |
Genomic and transcriptomic landscapes and evolutionary dynamics of molluscan glycoside hydrolase families with implications for algae-feeding biology |
title_sort |
genomic and transcriptomic landscapes and evolutionary dynamics of molluscan glycoside hydrolase families with implications for algae-feeding biology |
publisher |
Elsevier |
series |
Computational and Structural Biotechnology Journal |
issn |
2001-0370 |
publishDate |
2020-01-01 |
description |
The hydrolysis of sugar-containing compounds by glycoside hydrolases (GHs) plays essential roles in many major biological processes, but to date our systematic understanding of the functional diversity and evolution of GH families remains largely limited to a few well-studied terrestrial animals. Molluscs represent the largest marine phylum in the animal kingdom, and many of them are herbivorous that utilize algae as a main nutritional source, making them good subjects for studying the functional diversity and adaptive evolution of GH families. In the present study, we conducted genome-wide identification and functional and evolutionary analysis of all GH families across major molluscan lineages. We revealed that the remarkable expansion of the GH9, GH10, GH18 and GH20 families and the wide adoption of carbohydrate-binding modules in molluscan expanded GH families likely contributed to the efficient hydrolysis of marine algal polysaccharides and were involved in the consolidation of molluscan algae-feeding habits. Gene expression and network analysis revealed the hepatopancreas as the main organ for the prominent expression of approximately half of the GH families (well corresponding to the digestive roles of the hepatopancreas) and key or hub GHs in the coexpression gene network with potentially diverse functionalities. We also revealed the evolutionary signs of differential expansion and functional divergence of the GH family, which possibly contributed to lineage-specific adaptation. Systematic analysis of GH families at both genomic and transcriptomic levels provides important clues for understanding the functional divergence and evolution of GH gene families in molluscs in relation to their algae-feeding biology. |
topic |
Mollusc Glycoside hydrolase Gene family expansion Adaptive evolution Algae feeding |
url |
http://www.sciencedirect.com/science/article/pii/S2001037020304050 |
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doaj-b4c0a6332779474fbe2504894d96daf02021-01-02T05:09:04ZengElsevierComputational and Structural Biotechnology Journal2001-03702020-01-011827442756Genomic and transcriptomic landscapes and evolutionary dynamics of molluscan glycoside hydrolase families with implications for algae-feeding biologyJing Wang0Hongwei Yu1Lijie Yao2Yuli Li3Fuyun Liu4Wentao Han5Cong Cui6Jingjie Hu7Zhenmin Bao8Shi Wang9MOE Key Laboratory of Marine Genetics and Breeding and Sars-Fang Centre, Ocean University of China, Qingdao 266003, China; Laboratory for Marine Biology and Biotechnology, Pilot Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, ChinaMOE Key Laboratory of Marine Genetics and Breeding and Sars-Fang Centre, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding and Sars-Fang Centre, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding and Sars-Fang Centre, Ocean University of China, Qingdao 266003, China; Laboratory for Marine Biology and Biotechnology, Pilot Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China; Corresponding authors at: MOE Key Laboratory of Marine Genetics and Breeding and Sars-Fang Centre, Ocean University of China, Qingdao 266003, China.MOE Key Laboratory of Marine Genetics and Breeding and Sars-Fang Centre, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding and Sars-Fang Centre, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding and Sars-Fang Centre, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding and Sars-Fang Centre, Ocean University of China, Qingdao 266003, China; Laboratory of Tropical Marine Germplasm Resources and Breeding Engineering, Sanya Oceanographic Institution, Ocean University of China, Sanya 572000, ChinaMOE Key Laboratory of Marine Genetics and Breeding and Sars-Fang Centre, Ocean University of China, Qingdao 266003, China; Laboratory for Marine Fisheries Science and Food Production Processes, Pilot Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China; Laboratory of Tropical Marine Germplasm Resources and Breeding Engineering, Sanya Oceanographic Institution, Ocean University of China, Sanya 572000, ChinaMOE Key Laboratory of Marine Genetics and Breeding and Sars-Fang Centre, Ocean University of China, Qingdao 266003, China; Laboratory for Marine Biology and Biotechnology, Pilot Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China; Laboratory of Tropical Marine Germplasm Resources and Breeding Engineering, Sanya Oceanographic Institution, Ocean University of China, Sanya 572000, China; Corresponding authors at: MOE Key Laboratory of Marine Genetics and Breeding and Sars-Fang Centre, Ocean University of China, Qingdao 266003, China.The hydrolysis of sugar-containing compounds by glycoside hydrolases (GHs) plays essential roles in many major biological processes, but to date our systematic understanding of the functional diversity and evolution of GH families remains largely limited to a few well-studied terrestrial animals. Molluscs represent the largest marine phylum in the animal kingdom, and many of them are herbivorous that utilize algae as a main nutritional source, making them good subjects for studying the functional diversity and adaptive evolution of GH families. In the present study, we conducted genome-wide identification and functional and evolutionary analysis of all GH families across major molluscan lineages. We revealed that the remarkable expansion of the GH9, GH10, GH18 and GH20 families and the wide adoption of carbohydrate-binding modules in molluscan expanded GH families likely contributed to the efficient hydrolysis of marine algal polysaccharides and were involved in the consolidation of molluscan algae-feeding habits. Gene expression and network analysis revealed the hepatopancreas as the main organ for the prominent expression of approximately half of the GH families (well corresponding to the digestive roles of the hepatopancreas) and key or hub GHs in the coexpression gene network with potentially diverse functionalities. We also revealed the evolutionary signs of differential expansion and functional divergence of the GH family, which possibly contributed to lineage-specific adaptation. Systematic analysis of GH families at both genomic and transcriptomic levels provides important clues for understanding the functional divergence and evolution of GH gene families in molluscs in relation to their algae-feeding biology.http://www.sciencedirect.com/science/article/pii/S2001037020304050MolluscGlycoside hydrolaseGene family expansionAdaptive evolutionAlgae feeding |