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  • American Society for Microbiology  (19)
  • American Association for the Advancement of Science (AAAS)  (2)
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  • 1
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    Lifestyle evolution in cyanobacterial symbionts of sponges (2015)
    American Society for Microbiology
    Details
    Publication Date: 2022-05-25
    Description: © The Author(s), 2015. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in mBio 6 (2015): e00391-15, doi:10.1128/mBio.00391-15.
    Description: The “Candidatus Synechococcus spongiarum” group includes different clades of cyanobacteria with high 16S rRNA sequence identity (~99%) and is the most abundant and widespread cyanobacterial symbiont of marine sponges. The first draft genome of a “Ca. Synechococcus spongiarum” group member was recently published, providing evidence of genome reduction by loss of genes involved in several nonessential functions. However, “Ca. Synechococcus spongiarum” includes a variety of clades that may differ widely in genomic repertoire and consequently in physiology and symbiotic function. Here, we present three additional draft genomes of “Ca. Synechococcus spongiarum,” each from a different clade. By comparing all four symbiont genomes to those of free-living cyanobacteria, we revealed general adaptations to life inside sponges and specific adaptations of each phylotype. Symbiont genomes shared about half of their total number of coding genes. Common traits of “Ca. Synechococcus spongiarum” members were a high abundance of DNA modification and recombination genes and a reduction in genes involved in inorganic ion transport and metabolism, cell wall biogenesis, and signal transduction mechanisms. Moreover, these symbionts were characterized by a reduced number of antioxidant enzymes and low-weight peptides of photosystem II compared to their free-living relatives. Variability within the “Ca. Synechococcus spongiarum” group was mostly related to immune system features, potential for siderophore-mediated iron transport, and dependency on methionine from external sources. The common absence of genes involved in synthesis of residues, typical of the O antigen of free-living Synechococcus species, suggests a novel mechanism utilized by these symbionts to avoid sponge predation and phage attack.
    Description: Support for this study was provided by a USA-Israel Binational Science Foundation Young Investigator grant (BSF no. 4161011) to L.S. and a DOE Joint Genome Institute grant (CSP 1291) to U.H.; B.M.S. was supported by a grant of the German Excellence Initiative to the Graduate School of Life Sciences, University of Würzburg.
    Repository Name: Woods Hole Open Access Server
    Type: Article
    Format: application/pdf
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    PAPER (OA)
  • 2
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    Marine Sponges as Chloroflexi Hot Spots: Genomic Insights and High-Resolution Visualization of an Abundant and Diverse Symbiotic Clade (2018)
    American Society for Microbiology
    In:  mSystems, 3 (6). e00150-18.
    Details
    Publication Date: 2021-03-19
    Description: Members of the widespread bacterial phylum Chloroflexi can dominate high-microbial-abundance (HMA) sponge microbiomes. In the Sponge Microbiome Project, Chloroflexi sequences amounted to 20 to 30% of the total microbiome of certain HMA sponge genera with the classes/clades SAR202, Caldilineae, and Anaerolineae being the most prominent. We performed metagenomic and single-cell genomic analyses to elucidate the functional gene repertoire of Chloroflexi symbionts of Aplysina aerophoba. Eighteen draft genomes were reconstructed and placed into phylogenetic context of which six were investigated in detail. Common genomic features of Chloroflexi sponge symbionts were related to central energy and carbon converting pathways, amino acid and fatty acid metabolism, and respiration. Clade-specific metabolic features included a massively expanded genomic repertoire for carbohydrate degradation in Anaerolineae and Caldilineae genomes, but only amino acid utilization by SAR202. While Anaerolineae and Caldilineae import cofactors and vitamins, SAR202 genomes harbor genes encoding components involved in cofactor biosynthesis. A number of features relevant to symbiosis were further identified, including CRISPR-Cas systems, eukaryote-like repeat proteins, and secondary metabolite gene clusters. Chloroflexi symbionts were visualized in the sponge extracellular matrix at ultrastructural resolution by the fluorescence in situ hybridization-correlative light and electron microscopy (FISH-CLEM) method. Carbohydrate degradation potential was reported previously for “Candidatus Poribacteria” and SAUL, typical symbionts of HMA sponges, and we propose here that HMA sponge symbionts collectively engage in degradation of dissolved organic matter, both labile and recalcitrant. Thus, sponge microbes may not only provide nutrients to the sponge host, but they may also contribute to dissolved organic matter (DOM) recycling and primary productivity in reef ecosystems via a pathway termed the sponge loop. IMPORTANCE Chloroflexi represent a widespread, yet enigmatic bacterial phylum with few cultivated members. We used metagenomic and single-cell genomic approaches to characterize the functional gene repertoire of Chloroflexi symbionts in marine sponges. The results of this study suggest clade-specific metabolic specialization and that Chloroflexi symbionts have the genomic potential for dissolved organic matter (DOM) degradation from seawater. Considering the abundance and dominance of sponges in many benthic environments, we predict that the role of sponge symbionts in biogeochemical cycles is larger than previously thought.
    Type: Article , PeerReviewed , info:eu-repo/semantics/article
    Format: text
    DOI: 10.1128/mSystems.00150-18
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    OceanRep: Article in a Scientific Journal - peer-reviewed
  • 3
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    Mining Genomes of Three Marine Sponge-Associated Actinobacterial Isolates for Secondary Metabolism (2015)
    American Society for Microbiology
    In:  Genome Announcements, 3 (5). e01106-15.
    Details
    Publication Date: 2019-01-22
    Description: Here, we report the draft genome sequences of three actinobacterial isolates, Micromonospora sp. RV43, Rubrobacter sp. RV113, and Nocardiopsis sp. RV163 that had previously been isolated from Mediterranean sponges. The draft genomes were analyzed for the presence of gene clusters indicative of secondary metabolism using antiSMASH 3.0 and NapDos pipelines. Our findings demonstrated the chemical richness of sponge-associated actinomycetes and the efficacy of genome mining in exploring the genomic potential of sponge-derived actinomycetes.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1128/genomeA.01106-15
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    OceanRep: Article in a Scientific Journal - peer-reviewed
  • 4
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    Grapevine (Vitis vinifera) Crown Galls Host Distinct Microbiota (2016)
    American Society for Microbiology
    In:  Applied and Environmental Microbiology, 82 (18). pp. 5542-5552.
    Details
    Publication Date: 2019-02-01
    Description: Crown gall disease of grapevine is caused by virulent Agrobacterium strains and establishes a suitable habitat for agrobacteria and, potentially, other bacteria. The microbial community associated with grapevine plants has not been investigated with respect to this disease, which frequently results in monetary losses. This study compares the endophytic microbiota of organs from grapevine plants with or without crown gall disease and the surrounding vineyard soil over the growing seasons of 1 year. Amplicon-based community profiling revealed that the dominating factor causing differences between the grapevine microbiota is the sample site, not the crown gall disease. The soil showed the highest microbial diversity, which decreased with the distance from the soil over the root and the graft union of the trunk to the cane. Only the graft union microbiota was significantly affected by crown gall disease. The bacterial community of graft unions without a crown gall hosted transient microbiota, with the three most abundant bacterial species changing from season to season. In contrast, graft unions with a crown gall had a higher species richness, which in every season was dominated by the same three bacteria (Pseudomonas sp., Enterobacteriaceae sp., and Agrobacterium vitis). For in vitro-cultivated grapevine plantlets, A. vitis infection alone was sufficient to cause crown gall disease. Our data show that microbiota in crown galls is more stable over time than microbiota in healthy graft unions and that the microbial community is not essential for crown gall disease outbreak.
    Type: Article , PeerReviewed
    Format: text
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    DOI: 10.1128/AEM.01131-16
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    OceanRep: Article in a Scientific Journal - peer-reviewed
  • 5
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    Draft Genome Sequence of the Antitrypanosomally Active Sponge-Associated Bacterium Actinokineospora sp. Strain EG49 (2014)
    American Society for Microbiology
    In:  Genome Announcements, 2 (2). e00160-14.
    Details
    Publication Date: 2020-07-31
    Description: The marine sponge-associated bacterium Actinokineospora sp. strain EG49 produces the antitrypanosomal angucycline-like compound actinosporin A. The draft genome of Actinokineospora sp. EG49 has a size of 7.5 megabases and a GC content of 72.8% and contains 6,629 protein-coding sequences (CDS). antiSMASH predicted 996 genes residing in 36 secondary metabolite gene clusters.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1128/genomeA.00160-14
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    OceanRep: Article in a Scientific Journal - peer-reviewed
  • 6
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    Widespread Distribution of Poribacteria in Demospongiae (2009)
    American Society for Microbiology
    In:  Applied and Environmental Microbiology, 75 (17). pp. 5695-5699.
    Details
    Publication Date: 2015-07-03
    Description: Poribacteria were found in nine sponge species belonging to six orders of Porifera from three oceans. Phylogenetic analysis revealed four distinct poribacterial clades, which contained organisms obtained from several different geographic regions, indicating that the distribution of poribacteria is cosmopolitan. Members of divergent poribacterial clades were also found in the same sponge species in three different sponge genera.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1128/AEM.00035-09
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    OceanRep: Article in a Scientific Journal - peer-reviewed
  • 7
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    Lifestyle Evolution in Cyanobacterial Symbionts of Sponges (2015)
    American Society for Microbiology
    In:  mBio, 6 (3). e00391-15.
    Details
    Publication Date: 2020-04-20
    Description: The “Candidatus Synechococcus spongiarum” group includes different clades of cyanobacteria with high 16S rRNA sequence identity (~99%) and is the most abundant and widespread cyanobacterial symbiont of marine sponges. The first draft genome of a “Ca. Synechococcus spongiarum” group member was recently published, providing evidence of genome reduction by loss of genes involved in several nonessential functions. However, “Ca. Synechococcus spongiarum” includes a variety of clades that may differ widely in genomic repertoire and consequently in physiology and symbiotic function. Here, we present three additional draft genomes of “Ca. Synechococcus spongiarum,” each from a different clade. By comparing all four symbiont genomes to those of free-living cyanobacteria, we revealed general adaptations to life inside sponges and specific adaptations of each phylotype. Symbiont genomes shared about half of their total number of coding genes. Common traits of “Ca. Synechococcus spongiarum” members were a high abundance of DNA modification and recombination genes and a reduction in genes involved in inorganic ion transport and metabolism, cell wall biogenesis, and signal transduction mechanisms. Moreover, these symbionts were characterized by a reduced number of antioxidant enzymes and low-weight peptides of photosystem II compared to their free-living relatives. Variability within the “Ca. Synechococcus spongiarum” group was mostly related to immune system features, potential for siderophore-mediated iron transport, and dependency on methionine from external sources. The common absence of genes involved in synthesis of residues, typical of the O antigen of free-living Synechococcus species, suggests a novel mechanism utilized by these symbionts to avoid sponge predation and phage attack.
    Type: Article , PeerReviewed
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    DOI: 10.1128/mBio.00391-15
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    OceanRep: Article in a Scientific Journal - peer-reviewed
  • 8
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    Interaction of Legionella pneumophila with Dictyostelium discoideum (2002)
    American Society for Microbiology
    In:  In: Legionella. , ed. by Marre, R., Kwaik, Y. A. and Bartlett, C. Legionella : proceedings of the International Symposium on Legionella, 5 . American Society for Microbiology, Washington, USA, pp. 161-164. ISBN 1-555-81230-9
    Details
    Publication Date: 2016-06-28
    Type: Book chapter , PeerReviewed
    Format: text
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    OceanRep: Book chapter
  • 9
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    Molecular Microbial Diversity Survey of Sponge Reproductive Stages and Mechanistic Insights into Vertical Transmission of Microbial Symbionts (2008)
    American Society for Microbiology
    In:  Applied and Environmental Microbiology, 74 (24). pp. 7694-7708.
    Details
    Publication Date: 2015-07-03
    Description: Many marine sponges, hereafter termed high-microbial-abundance (HMA) sponges, harbor large and complex microbial consortia, including bacteria and archaea, within their mesohyl matrices. To investigate vertical microbial transmission as a strategy to maintain these complex associations, an extensive phylogenetic analysis was carried out with the 16S rRNA gene sequences of reproductive (n = 136) and adult (n = 88) material from five different Caribbean species, as well as all published 16S rRNA gene sequences from sponge offspring (n = 116). The overall microbial diversity, including members of at least 13 bacterial phyla and one archaeal phylum, in sponge reproductive stages is high. In total, 28 vertical-transmission clusters, defined as clusters of phylotypes that are found both in adult sponges and their offspring, were identified. They are distributed among at least 10 bacterial phyla and one archaeal phylum, demonstrating that the complex adult microbial community is collectively transmitted through reproductive stages. Indications of host-species specificity and cospeciation were not observed. Mechanistic insights were provided using a combined electron microscopy and fluorescence in situ hybridization analysis, and an indirect mechanism of vertical transmission via nurse cells is proposed for the oviparous sponge Ectyoplasia ferox. Based on these phylogenetic and mechanistic results, we suggest the following symbiont transmission model: entire microbial consortia are vertically transmitted in sponges. While vertical transmission is clearly present, additional environmental transfer between adult individuals of the same and even different species might obscure possible signals of cospeciation. We propose that associations of HMA sponges with highly sponge-specific microbial communities are maintained by this combination of vertical and horizontal symbiont transmission
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1128/AEM.00878-08
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    OceanRep: Article in a Scientific Journal - peer-reviewed
  • 10
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    Genetics: Evolutionary Insights from Sponges (2007)
    American Association for the Advancement of Science (AAAS)
    In:  Science, 316 (5833). pp. 1854-1855.
    Details
    Publication Date: 2020-10-21
    Description: Sponges (phylum Porifera) are among the most ancient of the multicellular animals, or Metazoa, with a fossil record dating back at least 580 million years (1). Found both in marine and freshwater environments, they filter-feed by pumping water through their bodies, which can contain a remarkable number of microbial symbionts. Sponges lack many of the characteristics typical of animals, but recent genomic studies—including the report by Jackson et al. on page 1893 of this issue (2)—have shown that they possess many major metazoan gene families. Sponges are thus invaluable systems for studying the evolution of metazoans and their interactions with microorganisms. Furthermore, their highly stable skeletons are of interest to materials scientists. Biomineralization is an important feature of metazoan life. Animals including vertebrates, insects, mollusks, and sponges use minerals [such as calcium carbonate, iron, and silica] to form skeletal structures such as bones, seashells, and coral reefs (3). Biocalcification arose among many metazoan lineages during the “Cambrian explosion,” between 530 and 520 million years ago, when the ancestors of today's animals first appeared in the fossil record. Did these lineages share the same gene(s) for biocalcification, or did multiple independent evolutionary events give rise to the ability to biocalcify? Recent studies, including that by Jackson et al., are beginning to provide an answer to this question. Jackson et al. use the Indo- Pacific sponge Astrosclera willeyana to show that the last common ancestor of the metazoans possessed a precursor to the α-carbonic anhydrases. This gene family is used by animals today in a range of processes including ion transport, pH regulation, and biomineralization (4). By integrating molecular techniques ranging from protein sequencing to gene expression, the authors identified a group of closely related α-carbonic anhydrase sequences in A. willeyana. These sequences are similar to those recovered from a whole-genome project on another sponge, Amphimedon queenslandica (5). Together, the sponge α-carbonic anhydrases form a sister group to those of all other metazoans.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1126/science.1144387
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    OceanRep: Article in a Scientific Journal - peer-reviewed
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