Genome Reduction and Secondary Metabolism of the Marine Sponge-Associated Cyanobacterium <i>Leptothoe</i>

Sponges form symbiotic relationships with diverse and abundant microbial communities. Cyanobacteria are among the most important members of the microbial communities that are associated with sponges. Here, we performed a genus-wide comparative genomic analysis of the newly described marine benthic c...

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Main Authors: Despoina Konstantinou, Rafael V. Popin, David P. Fewer, Kaarina Sivonen, Spyros Gkelis
Format: Article
Language:English
Published: MDPI AG 2021-05-01
Series:Marine Drugs
Subjects:
Online Access:https://www.mdpi.com/1660-3397/19/6/298
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author Despoina Konstantinou
Rafael V. Popin
David P. Fewer
Kaarina Sivonen
Spyros Gkelis
author_facet Despoina Konstantinou
Rafael V. Popin
David P. Fewer
Kaarina Sivonen
Spyros Gkelis
author_sort Despoina Konstantinou
collection DOAJ
description Sponges form symbiotic relationships with diverse and abundant microbial communities. Cyanobacteria are among the most important members of the microbial communities that are associated with sponges. Here, we performed a genus-wide comparative genomic analysis of the newly described marine benthic cyanobacterial genus <i>Leptothoe</i> (Synechococcales). We obtained draft genomes from <i>Le. kymatousa</i> TAU-MAC 1615 and <i>Le. spongobia</i> TAU-MAC 1115, isolated from marine sponges. We identified five additional <i>Leptothoe</i> genomes, host-associated or free-living, using a phylogenomic approach, and the comparison of all genomes showed that the sponge-associated strains display features of a symbiotic lifestyle. <i>Le. kymatousa</i> and <i>Le. spongobia</i> have undergone genome reduction; they harbored considerably fewer genes encoding for (i) cofactors, vitamins, prosthetic groups, pigments, proteins, and amino acid biosynthesis; (ii) DNA repair; (iii) antioxidant enzymes; and (iv) biosynthesis of capsular and extracellular polysaccharides. They have also lost several genes related to chemotaxis and motility. Eukaryotic-like proteins, such as ankyrin repeats, playing important roles in sponge-symbiont interactions, were identified in sponge-associated <i>Leptothoe</i> genomes. The sponge-associated <i>Leptothoe</i> stains harbored biosynthetic gene clusters encoding novel natural products despite genome reduction. Comparisons of the biosynthetic capacities of <i>Leptothoe</i> with chemically rich cyanobacteria revealed that <i>Leptothoe</i> is another promising marine cyanobacterium for the biosynthesis of novel natural products.
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spelling doaj.art-7b995f675e49403eb74bcec42c82b6a22023-11-21T21:05:13ZengMDPI AGMarine Drugs1660-33972021-05-0119629810.3390/md19060298Genome Reduction and Secondary Metabolism of the Marine Sponge-Associated Cyanobacterium <i>Leptothoe</i>Despoina Konstantinou0Rafael V. Popin1David P. Fewer2Kaarina Sivonen3Spyros Gkelis4Department of Botany, School of Biology, Aristotle University of Thessaloniki, GR-541 24 Thessaloniki, GreeceDepartment of Microbiology, University of Helsinki, Viikinkaari 9, FI-00014 Helsinki, FinlandDepartment of Microbiology, University of Helsinki, Viikinkaari 9, FI-00014 Helsinki, FinlandDepartment of Microbiology, University of Helsinki, Viikinkaari 9, FI-00014 Helsinki, FinlandDepartment of Botany, School of Biology, Aristotle University of Thessaloniki, GR-541 24 Thessaloniki, GreeceSponges form symbiotic relationships with diverse and abundant microbial communities. Cyanobacteria are among the most important members of the microbial communities that are associated with sponges. Here, we performed a genus-wide comparative genomic analysis of the newly described marine benthic cyanobacterial genus <i>Leptothoe</i> (Synechococcales). We obtained draft genomes from <i>Le. kymatousa</i> TAU-MAC 1615 and <i>Le. spongobia</i> TAU-MAC 1115, isolated from marine sponges. We identified five additional <i>Leptothoe</i> genomes, host-associated or free-living, using a phylogenomic approach, and the comparison of all genomes showed that the sponge-associated strains display features of a symbiotic lifestyle. <i>Le. kymatousa</i> and <i>Le. spongobia</i> have undergone genome reduction; they harbored considerably fewer genes encoding for (i) cofactors, vitamins, prosthetic groups, pigments, proteins, and amino acid biosynthesis; (ii) DNA repair; (iii) antioxidant enzymes; and (iv) biosynthesis of capsular and extracellular polysaccharides. They have also lost several genes related to chemotaxis and motility. Eukaryotic-like proteins, such as ankyrin repeats, playing important roles in sponge-symbiont interactions, were identified in sponge-associated <i>Leptothoe</i> genomes. The sponge-associated <i>Leptothoe</i> stains harbored biosynthetic gene clusters encoding novel natural products despite genome reduction. Comparisons of the biosynthetic capacities of <i>Leptothoe</i> with chemically rich cyanobacteria revealed that <i>Leptothoe</i> is another promising marine cyanobacterium for the biosynthesis of novel natural products.https://www.mdpi.com/1660-3397/19/6/298cyanobacteriasymbiontsmarine spongescomparative genomicsnatural productsbiosynthetic gene clusters
spellingShingle Despoina Konstantinou
Rafael V. Popin
David P. Fewer
Kaarina Sivonen
Spyros Gkelis
Genome Reduction and Secondary Metabolism of the Marine Sponge-Associated Cyanobacterium <i>Leptothoe</i>
Marine Drugs
cyanobacteria
symbionts
marine sponges
comparative genomics
natural products
biosynthetic gene clusters
title Genome Reduction and Secondary Metabolism of the Marine Sponge-Associated Cyanobacterium <i>Leptothoe</i>
title_full Genome Reduction and Secondary Metabolism of the Marine Sponge-Associated Cyanobacterium <i>Leptothoe</i>
title_fullStr Genome Reduction and Secondary Metabolism of the Marine Sponge-Associated Cyanobacterium <i>Leptothoe</i>
title_full_unstemmed Genome Reduction and Secondary Metabolism of the Marine Sponge-Associated Cyanobacterium <i>Leptothoe</i>
title_short Genome Reduction and Secondary Metabolism of the Marine Sponge-Associated Cyanobacterium <i>Leptothoe</i>
title_sort genome reduction and secondary metabolism of the marine sponge associated cyanobacterium i leptothoe i
topic cyanobacteria
symbionts
marine sponges
comparative genomics
natural products
biosynthetic gene clusters
url https://www.mdpi.com/1660-3397/19/6/298
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