Phylogenetic analysis, metabolic profiling, and environmental adaptation of strain LCG007: a novel Rhodobacteraceae isolated from the East China Sea intertidal zone

Strain LCG007, isolated from Lu Chao Harbor's intertidal water, phylogenetically represents a novel genus within the family Rhodobacteraceae. Metabolically, it possesses a wide array of amino acid metabolic genes that enable it to thrive on both amino acids or peptides. Also, it could hydrolyze...

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Main Authors: Cuizhu Liang, Jiahua Wang, Jie Liu, Zekai Wang, Junwei Cao, Xi Yu, Li Zhang, Jiasong Fang
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2024.1533195/full
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author Cuizhu Liang
Jiahua Wang
Jie Liu
Zekai Wang
Junwei Cao
Xi Yu
Li Zhang
Jiasong Fang
Jiasong Fang
author_facet Cuizhu Liang
Jiahua Wang
Jie Liu
Zekai Wang
Junwei Cao
Xi Yu
Li Zhang
Jiasong Fang
Jiasong Fang
author_sort Cuizhu Liang
collection DOAJ
description Strain LCG007, isolated from Lu Chao Harbor's intertidal water, phylogenetically represents a novel genus within the family Rhodobacteraceae. Metabolically, it possesses a wide array of amino acid metabolic genes that enable it to thrive on both amino acids or peptides. Also, it could hydrolyze peptides containing D-amino acids, highlighting its potential role in the cycling of refractory organic matter. Moreover, strain LCG007 could utilize various carbohydrates, including mannopine and D-apiose—compounds primarily derived from terrestrial plants—demonstrating its capacity to degrade terrestrial organic matter. It could assimilate ammonia, nitrate and nitrite, and utilizes organic nitrogen sources such as polyamines, along with diverse organic and inorganic phosphorus and sulfur sources. Importantly, unlike very limited Sulfitobacter species that possess photosynthetic genes, the genomes of strain LCG007-affiliated genus and all Roseobacter species harbor photosynthetic gene clusters. This conservation was further supported by the significant impact of light on the growth and cell aggregation of strain LCG007, suggesting that acquirement of photosynthetic genes could play a crucial role in the speciation of their common ancestor. In terms of environmental adaptability, the genes that encode for DNA photolyase, heat and cold shock proteins, and enzymes responsible for scavenging reactive oxygen species, along with those involved in the uptake and biosynthesis of osmoprotectants such as betaine, γ-aminobutyric acid (GABA), and trehalose collectively enable strain LCG007 to survive in the dynamic and complex intertidal zone environment. Besides, the capacity in biofilm formation is crucial for its survival under conditions of oligotrophy or high salinity. This study enhances our comprehension of the microbial taxonomy within the Roseobacter clade affiliated cluster, their survival strategies in intertidal ecosystems, and underscores the significance of their role in nutrient cycling. It also highlights the crucial importance of photosynthetic metabolism for the speciation of marine bacteria and their ecological resilience.
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spelling doaj-art-d7238a98b93145f7a49348782790af542025-01-07T06:45:06ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-01-011510.3389/fmicb.2024.15331951533195Phylogenetic analysis, metabolic profiling, and environmental adaptation of strain LCG007: a novel Rhodobacteraceae isolated from the East China Sea intertidal zoneCuizhu Liang0Jiahua Wang1Jie Liu2Zekai Wang3Junwei Cao4Xi Yu5Li Zhang6Jiasong Fang7Jiasong Fang8Shanghai Engineering Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean University, Shanghai, ChinaShanghai Engineering Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean University, Shanghai, ChinaShanghai Engineering Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean University, Shanghai, ChinaShanghai Engineering Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean University, Shanghai, ChinaShanghai Engineering Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean University, Shanghai, ChinaShanghai Engineering Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean University, Shanghai, ChinaShanghai Engineering Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean University, Shanghai, ChinaShanghai Engineering Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean University, Shanghai, ChinaLaboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaStrain LCG007, isolated from Lu Chao Harbor's intertidal water, phylogenetically represents a novel genus within the family Rhodobacteraceae. Metabolically, it possesses a wide array of amino acid metabolic genes that enable it to thrive on both amino acids or peptides. Also, it could hydrolyze peptides containing D-amino acids, highlighting its potential role in the cycling of refractory organic matter. Moreover, strain LCG007 could utilize various carbohydrates, including mannopine and D-apiose—compounds primarily derived from terrestrial plants—demonstrating its capacity to degrade terrestrial organic matter. It could assimilate ammonia, nitrate and nitrite, and utilizes organic nitrogen sources such as polyamines, along with diverse organic and inorganic phosphorus and sulfur sources. Importantly, unlike very limited Sulfitobacter species that possess photosynthetic genes, the genomes of strain LCG007-affiliated genus and all Roseobacter species harbor photosynthetic gene clusters. This conservation was further supported by the significant impact of light on the growth and cell aggregation of strain LCG007, suggesting that acquirement of photosynthetic genes could play a crucial role in the speciation of their common ancestor. In terms of environmental adaptability, the genes that encode for DNA photolyase, heat and cold shock proteins, and enzymes responsible for scavenging reactive oxygen species, along with those involved in the uptake and biosynthesis of osmoprotectants such as betaine, γ-aminobutyric acid (GABA), and trehalose collectively enable strain LCG007 to survive in the dynamic and complex intertidal zone environment. Besides, the capacity in biofilm formation is crucial for its survival under conditions of oligotrophy or high salinity. This study enhances our comprehension of the microbial taxonomy within the Roseobacter clade affiliated cluster, their survival strategies in intertidal ecosystems, and underscores the significance of their role in nutrient cycling. It also highlights the crucial importance of photosynthetic metabolism for the speciation of marine bacteria and their ecological resilience.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1533195/fullintertidal zoneRCA clusterbiogeochemical cyclingenvironmental adaptationsmetabolic versatility
spellingShingle Cuizhu Liang
Jiahua Wang
Jie Liu
Zekai Wang
Junwei Cao
Xi Yu
Li Zhang
Jiasong Fang
Jiasong Fang
Phylogenetic analysis, metabolic profiling, and environmental adaptation of strain LCG007: a novel Rhodobacteraceae isolated from the East China Sea intertidal zone
Frontiers in Microbiology
intertidal zone
RCA cluster
biogeochemical cycling
environmental adaptations
metabolic versatility
title Phylogenetic analysis, metabolic profiling, and environmental adaptation of strain LCG007: a novel Rhodobacteraceae isolated from the East China Sea intertidal zone
title_full Phylogenetic analysis, metabolic profiling, and environmental adaptation of strain LCG007: a novel Rhodobacteraceae isolated from the East China Sea intertidal zone
title_fullStr Phylogenetic analysis, metabolic profiling, and environmental adaptation of strain LCG007: a novel Rhodobacteraceae isolated from the East China Sea intertidal zone
title_full_unstemmed Phylogenetic analysis, metabolic profiling, and environmental adaptation of strain LCG007: a novel Rhodobacteraceae isolated from the East China Sea intertidal zone
title_short Phylogenetic analysis, metabolic profiling, and environmental adaptation of strain LCG007: a novel Rhodobacteraceae isolated from the East China Sea intertidal zone
title_sort phylogenetic analysis metabolic profiling and environmental adaptation of strain lcg007 a novel rhodobacteraceae isolated from the east china sea intertidal zone
topic intertidal zone
RCA cluster
biogeochemical cycling
environmental adaptations
metabolic versatility
url https://www.frontiersin.org/articles/10.3389/fmicb.2024.1533195/full
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