Horizontal Gene Transfer Contributed to the Evolution of Extracellular Surface Structures: The Freshwater Polyp Hydra Is Covered by a Complex Fibrous Cuticle Containing Glycosaminoglycans and Proteins of the PPOD and SWT (Sweet Tooth) Families

Böttger, Angelika; Doxey, Andrew C.; Hess, Michael W.; Pfaller, Kristian; Salvenmoser, Willi; Deutzmann, Rainer; Geissner, Andreas; Pauly, Barbara; Altstätter, Johannes; Münder, Sandra; Heim, Astrid; Gabius, Hans‐Joachim; McConkey, Brendan J.; David, Charles N.

doi:10.1371/journal.pone.0052278

Cited by 28 publications

(41 citation statements)

References 48 publications

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“…The Hydra ectoderm is covered by a multilayered glycocalyx that is a habitat for a complex bacterial community Using HPF/FS we first confirmed earlier observations (Holstein et al, 2010;Bö ttger et al, 2012) that the Hydra ectoderm is covered by a multilayered glycocalyx. Transmission electron microscopy revealed five distinct layers (c1-5) in the glycocalyx that together extend up to 1.5 mm from the cell surface ( Figure 1b).…”

Section: Resultssupporting

confidence: 81%

Bacteria–bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance

et al. 2014

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Epithelial surfaces of most animals are colonized by diverse microbial communities. Although it is generally agreed that commensal bacteria can serve beneficial functions, the processes involved are poorly understood. Here we report that in the basal metazoan Hydra, ectodermal epithelial cells are covered with a multilayered glycocalyx that provides a habitat for a distinctive microbial community. Removing this epithelial microbiota results in lethal infection by the filamentous fungus Fusarium sp. Restoring the complex microbiota in gnotobiotic polyps prevents pathogen infection. Although mono-associations with distinct members of the microbiota fail to provide full protection, additive and synergistic interactions of commensal bacteria are contributing to full fungal resistance. Our results highlight the importance of resident microbiota diversity as a protective factor against pathogen infections. Besides revealing insights into the in vivo function of commensal microbes in Hydra, our findings indicate that interactions among commensal bacteria are essential to inhibit pathogen infection.

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Section: Resultssupporting

confidence: 81%

Bacteria–bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance

et al. 2014

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“…Invading microorganisms first have to overcome the physicochemical barrier represented by the multilayered glycocalyx that covers the ectodermal epithelium (27, 28). Complex cellular and humoral pathways represent the second arm of Hydra ’s immunity (29).…”

Section: Microbe-epithelial Interactions In Hydramentioning

confidence: 99%

“…2C) (27, 28). All layers of Hydra ’s glycocalyx, as well as the large secretory vesicles underneath the apical membrane, were shown to be highly periodic acid-Schiff stain (PAS) reactive, indicating a high carbohydrate content (28). Although the structure was initially termed glycocalyx, the characteristic feature of being membrane bound does not account for all of its layers.…”

Section: Hydra’s Glycocalyx and Mucus Layer: Both A Physicochemical Bmentioning

confidence: 99%

“…The outer layer (o), which accounts for more than 50% of the glycocalyx, is made of a loose meshwork that can be removed completely by a hypertonic salt wash. In contrast, the four inner layers (s) display a dense composition and are firmly attached to the epithelial surface (28). Therefore, we propose that the outer layer of Hydra ’s glycocalyx has mucuslike properties rather than being a part of the membrane-anchored glycocalyx.…”

Section: Hydra’s Glycocalyx and Mucus Layer: Both A Physicochemical Bmentioning

confidence: 99%

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The Origin of Mucosal Immunity: Lessons from the Holobiont Hydra

Schröder

Bosch

2016

mBio

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Historically, mucosal immunity—i.e., the portion of the immune system that protects an organism’s various mucous membranes from invasion by potentially pathogenic microbes—has been studied in single-cell epithelia in the gastrointestinal and upper respiratory tracts of vertebrates. Phylogenetically, mucosal surfaces appeared for the first time about 560 million years ago in members of the phylum Cnidaria. There are remarkable similarities and shared functions of mucosal immunity in vertebrates and innate immunity in cnidarians, such as Hydra species. Here, we propose a common origin for both systems and review observations that indicate that the ultimately simple holobiont Hydra provides both a new perspective on the relationship between bacteria and animal cells and a new prism for viewing the emergence and evolution of epithelial tissue-based innate immunity. In addition, recent breakthroughs in our understanding of immune responses in Hydra polyps reared under defined short-term gnotobiotic conditions open up the potential of Hydra as an animal research model for the study of common mucosal disorders.

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“…Sequence similarity based genome survey, phylogeny, correlation of gene and phenotype Chapman et al 2010;Böttger et al 2012 Silkmoth Bombyx mori Bacteria, plant, fungi Ten enzymes Sequence similarity Zhu et al 2011;Wheeler et al 2013 Gall midges including Asteromyia carbonifera Fungal Carotenoid biosynthesis gene homologues: one lycopene cyclase/phytoene synthase and two phytoene desaturase homologues Transcriptomics, PCR, phylogeny Cobbs et al 2013 Spider mite Tetranychus uriticae Fungal Carotenoid biosynthesis gene homologues cyanase Phylogeny Grbić et al 2011;Wybouw et al 2012;Wybouw et al 2014 Coffee borer beetle Hypothenemus hampei …”

Section: Animal Recipient Donor Organism Sequence Transferred Detectimentioning

confidence: 99%

Horizontal gene transfer in the sponge Amphimedon queenslandica

Higgie¹

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Horizontal gene transfer (HGT) is the nonsexual transfer of genetic sequence across species boundaries.Historically, HGT has been assumed largely irrelevant to animal evolution, though widely recognised as an important evolutionary force in bacteria. From the recent boom in whole genome sequencing, many cases have emerged strongly supporting the occurrence of HGT in a wide range of animals.However, the extent, nature and mechanisms of HGT in animals remain poorly understood. Here, I explore these uncertainties using 576 HGTs previously reported in the genome of the demosponge Amphimedon queenslandica.The HGTs derive from bacterial, plant and fungal sources, contain a broad range of domain types, and many are differentially expressed throughout development. Some domains are highly enriched; phylogenetic analyses of the two largest groups, the Aspzincin_M35 and the PNP_UDP_1 domain groups, suggest that each results from one or few transfer events followed by post-transfer duplication.Their differential expression through development, and the conservation of domains and duplicates, together suggest that many of the HGT-derived genes are functioning in A. queenslandica. The largest group consists of aspzincins, a metallopeptidase found in bacteria and fungi, but not typically in animals.I detected aspzincins in representatives of all four of the sponge classes, suggesting that the original sponge aspzincin was transferred after sponges diverged from their last common ancestor with the Eumetazoa, but before the contemporary sponge classes emerged. In A. queenslandica, the aspzincins may have been co-opted for multiple functions, since 54 of the 90 fit into one of four ontogenetic expression profiles, each of which is putatively co-expressed with different suites of native genes.Based on secretion signals and the conservation of key catalytic residues, I propose that proteolytic activity is maintained in at least one of the aspzincin roles in A. queenslandica.Mobile elements are capable of genomic excision, movement and integration, they enable HGT in bacteria, and some animal HGTs are genomically close to eukaryotic transposable elements (TEs); as such, mobile elements are speculated as possible players in the mechanisms of interkingdom and interdomain HGT to animals. In A. queenslandica, the overall repeats densities around predicted Together, these results offer novel insight on HGT in A. queenslandica and demonstrate that HGT has a varied nature in this animal with an extensive impact, partially due to post-transfer duplications. Further, this work offers insights on possible mechanisms that led to the HGT derived genes of this sponge. iv Declaration by authorThis thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis.

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Horizontal Gene Transfer Contributed to the Evolution of Extracellular Surface Structures: The Freshwater Polyp Hydra Is Covered by a Complex Fibrous Cuticle Containing Glycosaminoglycans and Proteins of the PPOD and SWT (Sweet Tooth) Families

Cited by 28 publications

References 48 publications

Bacteria–bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance

Bacteria–bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance

The Origin of Mucosal Immunity: Lessons from the Holobiont Hydra

Horizontal gene transfer in the sponge Amphimedon queenslandica

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