Symbiotic Adaptation Drives Genome Streamlining of the Cyanobacterial Sponge Symbiont “<italic toggle="yes">Candidatus</italic> Synechococcus spongiarum”

ABSTRACT “Candidatus Synechococcus spongiarum” is a cyanobacterial symbiont widely distributed in sponges, but its functions at the genome level remain unknown. Here, we obtained the draft genome (1.66 Mbp, 90% estimated genome recovery) of “Ca. Synechococcus spongiarum” strain SH4 inhabiting the Re...

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Main Authors: Zhao-Ming Gao, Yong Wang, Ren-Mao Tian, Yue Him Wong, Zenon B. Batang, Abdulaz M. Al-Suwailem, Vladimir B. Bajic, Pei-Yuan Qian
Format: Article
Language:English
Published: American Society for Microbiology 2014-05-01
Series:mBio
Online Access:https://journals.asm.org/doi/10.1128/mBio.00079-14
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author Zhao-Ming Gao
Yong Wang
Ren-Mao Tian
Yue Him Wong
Zenon B. Batang
Abdulaz M. Al-Suwailem
Vladimir B. Bajic
Pei-Yuan Qian
author_facet Zhao-Ming Gao
Yong Wang
Ren-Mao Tian
Yue Him Wong
Zenon B. Batang
Abdulaz M. Al-Suwailem
Vladimir B. Bajic
Pei-Yuan Qian
author_sort Zhao-Ming Gao
collection DOAJ
description ABSTRACT “Candidatus Synechococcus spongiarum” is a cyanobacterial symbiont widely distributed in sponges, but its functions at the genome level remain unknown. Here, we obtained the draft genome (1.66 Mbp, 90% estimated genome recovery) of “Ca. Synechococcus spongiarum” strain SH4 inhabiting the Red Sea sponge Carteriospongia foliascens. Phylogenomic analysis revealed a high dissimilarity between SH4 and free-living cyanobacterial strains. Essential functions, such as photosynthesis, the citric acid cycle, and DNA replication, were detected in SH4. Eukaryoticlike domains that play important roles in sponge-symbiont interactions were identified exclusively in the symbiont. However, SH4 could not biosynthesize methionine and polyamines and had lost partial genes encoding low-molecular-weight peptides of the photosynthesis complex, antioxidant enzymes, DNA repair enzymes, and proteins involved in resistance to environmental toxins and in biosynthesis of capsular and extracellular polysaccharides. These genetic modifications imply that “Ca. Synechococcus spongiarum” SH4 represents a low-light-adapted cyanobacterial symbiont and has undergone genome streamlining to adapt to the sponge’s mild intercellular environment. IMPORTANCE Although the diversity of sponge-associated microbes has been widely studied, genome-level research on sponge symbionts and their symbiotic mechanisms is rare because they are unculturable. “Candidatus Synechococcus spongiarum” is a widely distributed uncultivated cyanobacterial sponge symbiont. The genome of this symbiont will help to characterize its evolutionary relationship and functional dissimilarity to closely related free-living cyanobacterial strains. Knowledge of its adaptive mechanism to the sponge host also depends on the genome-level research. The data presented here provided an alternative strategy to obtain the draft genome of “Ca. Synechococcus spongiarum” strain SH4 and provide insight into its evolutionary and functional features.
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spelling doaj.art-312274bd17584193952d608d70e9ca0d2022-12-21T19:08:53ZengAmerican Society for MicrobiologymBio2150-75112014-05-015210.1128/mBio.00079-14Symbiotic Adaptation Drives Genome Streamlining of the Cyanobacterial Sponge Symbiont “<italic toggle="yes">Candidatus</italic> Synechococcus spongiarum”Zhao-Ming Gao0Yong Wang1Ren-Mao Tian2Yue Him Wong3Zenon B. Batang4Abdulaz M. Al-Suwailem5Vladimir B. Bajic6Pei-Yuan Qian7KAUST Global Collaborative Research Program, Division of Life Science, The Hong Kong University of Science and Technology, Kowloon, Hong Kong, People’s Republic of ChinaKAUST Global Collaborative Research Program, Division of Life Science, The Hong Kong University of Science and Technology, Kowloon, Hong Kong, People’s Republic of ChinaKAUST Global Collaborative Research Program, Division of Life Science, The Hong Kong University of Science and Technology, Kowloon, Hong Kong, People’s Republic of ChinaKAUST Global Collaborative Research Program, Division of Life Science, The Hong Kong University of Science and Technology, Kowloon, Hong Kong, People’s Republic of ChinaCoastal and Marine Resources Core Laboratory, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaCoastal and Marine Resources Core Laboratory, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaComputational Bioscience Research Center (CBRC) and Computer, Electrical and Mathematical Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaKAUST Global Collaborative Research Program, Division of Life Science, The Hong Kong University of Science and Technology, Kowloon, Hong Kong, People’s Republic of ChinaABSTRACT “Candidatus Synechococcus spongiarum” is a cyanobacterial symbiont widely distributed in sponges, but its functions at the genome level remain unknown. Here, we obtained the draft genome (1.66 Mbp, 90% estimated genome recovery) of “Ca. Synechococcus spongiarum” strain SH4 inhabiting the Red Sea sponge Carteriospongia foliascens. Phylogenomic analysis revealed a high dissimilarity between SH4 and free-living cyanobacterial strains. Essential functions, such as photosynthesis, the citric acid cycle, and DNA replication, were detected in SH4. Eukaryoticlike domains that play important roles in sponge-symbiont interactions were identified exclusively in the symbiont. However, SH4 could not biosynthesize methionine and polyamines and had lost partial genes encoding low-molecular-weight peptides of the photosynthesis complex, antioxidant enzymes, DNA repair enzymes, and proteins involved in resistance to environmental toxins and in biosynthesis of capsular and extracellular polysaccharides. These genetic modifications imply that “Ca. Synechococcus spongiarum” SH4 represents a low-light-adapted cyanobacterial symbiont and has undergone genome streamlining to adapt to the sponge’s mild intercellular environment. IMPORTANCE Although the diversity of sponge-associated microbes has been widely studied, genome-level research on sponge symbionts and their symbiotic mechanisms is rare because they are unculturable. “Candidatus Synechococcus spongiarum” is a widely distributed uncultivated cyanobacterial sponge symbiont. The genome of this symbiont will help to characterize its evolutionary relationship and functional dissimilarity to closely related free-living cyanobacterial strains. Knowledge of its adaptive mechanism to the sponge host also depends on the genome-level research. The data presented here provided an alternative strategy to obtain the draft genome of “Ca. Synechococcus spongiarum” strain SH4 and provide insight into its evolutionary and functional features.https://journals.asm.org/doi/10.1128/mBio.00079-14
spellingShingle Zhao-Ming Gao
Yong Wang
Ren-Mao Tian
Yue Him Wong
Zenon B. Batang
Abdulaz M. Al-Suwailem
Vladimir B. Bajic
Pei-Yuan Qian
Symbiotic Adaptation Drives Genome Streamlining of the Cyanobacterial Sponge Symbiont “<italic toggle="yes">Candidatus</italic> Synechococcus spongiarum”
mBio
title Symbiotic Adaptation Drives Genome Streamlining of the Cyanobacterial Sponge Symbiont “<italic toggle="yes">Candidatus</italic> Synechococcus spongiarum”
title_full Symbiotic Adaptation Drives Genome Streamlining of the Cyanobacterial Sponge Symbiont “<italic toggle="yes">Candidatus</italic> Synechococcus spongiarum”
title_fullStr Symbiotic Adaptation Drives Genome Streamlining of the Cyanobacterial Sponge Symbiont “<italic toggle="yes">Candidatus</italic> Synechococcus spongiarum”
title_full_unstemmed Symbiotic Adaptation Drives Genome Streamlining of the Cyanobacterial Sponge Symbiont “<italic toggle="yes">Candidatus</italic> Synechococcus spongiarum”
title_short Symbiotic Adaptation Drives Genome Streamlining of the Cyanobacterial Sponge Symbiont “<italic toggle="yes">Candidatus</italic> Synechococcus spongiarum”
title_sort symbiotic adaptation drives genome streamlining of the cyanobacterial sponge symbiont italic toggle yes candidatus italic synechococcus spongiarum
url https://journals.asm.org/doi/10.1128/mBio.00079-14
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