Sexual reproduction in four Caribbean commercial sponges. II. Oogenesis and transfer of bacterial symbionts

Kaye, Heather R.

doi:10.1080/07924259.1991.9672152

Cited by 55 publications

(44 citation statements)

References 10 publications

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“…Such filamentous structures were previously described, e.g., the enveloping embryos of Spongia sp. and Hippospongia lachne (22) as well as Latrunculia magnifica (21). Ilan (21) suggested that the fibrils are secreted by a layer of sponge cells.…”

Section: Discussionmentioning

confidence: 99%

Molecular Microbial Diversity Survey of Sponge Reproductive Stages and Mechanistic Insights into Vertical Transmission of Microbial Symbionts

Schmitt¹,

Angermeier²,

Schiller³

et al. 2008

Appl Environ Microbiol

168

156

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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.Sponges (phylum Porifera) are evolutionarily ancient Metazoa whose origin dates back about 600 million years to the Precambrian (26). With 7,000 formally described species and an estimated 15,000 extant species, sponges are among the most diverse marine invertebrate groups and are important components of all aquatic habitats, including freshwater environments, tropical reefs, and even the deep sea (19). Despite an enormous range of shapes, colors, and sizes, all sponges possess a relatively simple body plan which is adapted to a filter-feeding lifestyle (4). Large volumes of seawater are pumped through canals embedded in an extracellular matrix (55), termed the mesohyl, and microorganisms and small unicellular eukaryotes are taken up from the seawater with high efficiency, leaving the expelled water essentially sterile (37, 54).Numerous sponges live in permanent and close associations with microorganisms, and many of them host phylogenetically diverse populations of microbes (15,17,49). These microorganisms are located mainly extracellularly in the sponge mesohyl in high concentrations, contributing up to 40% of the sponge's biomass and...

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Section: Discussionmentioning

confidence: 99%

Molecular Microbial Diversity Survey of Sponge Reproductive Stages and Mechanistic Insights into Vertical Transmission of Microbial Symbionts

Schmitt¹,

Angermeier²,

Schiller³

et al. 2008

Appl Environ Microbiol

168

156

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“…Sexual reproduction in sponges involves either vivipary (where larvae are brooded within the animal) or ovipary (whereby eggs, generally fertilized externally, develop outside the sponge). Evidence for vertical transmission of bacteria has been reported for both types (97,116,118,181,362,419,422,431), while asexual reproduction, i.e., budding, could also contribute to symbiont transfer in some species (146). Indeed, gemmules, the asexual buds of freshwater sponges, contain symbiotic zoochlorellae in at least some species (372), while a bud protruding from the surface of the marine sponge Tethya orphei contained a symbiotic cyanobacterium (117).…”

Section: Ecological Aspects: From Single Cells To the Global Scale Esmentioning

confidence: 99%

Sponge-Associated Microorganisms: Evolution, Ecology, and Biotechnological Potential

Taylor

Radax

Steger

et al. 2007

Microbiol Mol Biol Rev

1,295

1,512

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SUMMARY Marine sponges often contain diverse and abundant microbial communities, including bacteria, archaea, microalgae, and fungi. In some cases, these microbial associates comprise as much as 40% of the sponge volume and can contribute significantly to host metabolism (e.g., via photosynthesis or nitrogen fixation). We review in detail the diversity of microbes associated with sponges, including extensive 16S rRNA-based phylogenetic analyses which support the previously suggested existence of a sponge-specific microbiota. These analyses provide a suitable vantage point from which to consider the potential evolutionary and ecological ramifications of these widespread, sponge-specific microorganisms. Subsequently, we examine the ecology of sponge-microbe associations, including the establishment and maintenance of these sometimes intimate partnerships, the varied nature of the interactions (ranging from mutualism to host-pathogen relationships), and the broad-scale patterns of symbiont distribution. The ecological and evolutionary importance of sponge-microbe associations is mirrored by their enormous biotechnological potential: marine sponges are among the animal kingdom's most prolific producers of bioactive metabolites, and in at least some cases, the compounds are of microbial rather than sponge origin. We review the status of this important field, outlining the various approaches (e.g., cultivation, cell separation, and metagenomics) which have been employed to access the chemical wealth of sponge-microbe associations.

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“…Since then, vertical transmission of bacterial symbionts via eggs or larvae has been documented for several sponge species, including Tethya citrina (15), Geodia cydonium (50), Stelletta grubii (49), Hippospongia sp. (25), Spongia sp. (25), Halisarca dujardini (10), and Corticium candelabrum (8).…”

mentioning

confidence: 99%

“…(25), Spongia sp. (25), Halisarca dujardini (10), and Corticium candelabrum (8). However, all of these studies employed transmission and scanning electron microscopy and could only examine the presence of bacteria in maternal sponges, oocytes, or larvae at the morphological level, with no determination of microbial identity.…”

mentioning

confidence: 99%

Evidence for Vertical Transmission of Bacterial Symbionts from Adult to Embryo in the Caribbean SpongeSvenzea zeai

Lee

Chui

Wong

et al. 2009

Appl Environ Microbiol

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The Caribbean reef sponge Svenzea zeai was previously found to contain substantial quantities of unicellular photosynthetic and autotrophic microbes in its tissues, but the identities of these symbionts and their method of transfer from adult to progeny are largely unknown. In this study, both a 16S rRNA gene-based fingerprinting technique (denaturing gradient gel electrophoresis [DGGE]) and clone library analysis were applied to compare the bacterial communities associated with adults and embryos of S. zeai to test the hypothesis of vertical transfer across generations. In addition, the same techniques were applied to the bacterial community from the seawater adjacent to adult sponges to test the hypothesis that water column bacteria could be transferred horizontally as sponge symbionts. Results of both DGGE and clone library analysis support the vertical transfer hypothesis in that the bacterial communities associated with sponge adults and embryos were highly similar to each other but completely different from those in the surrounding seawater. Sequencing of prominent DGGE bands and of clones from the libraries revealed that the bacterial communities associated with the sponge, whether adult or embryo, consisted of a large proportion of bacteria in the phyla Chloroflexi and Acidobacteria, while most of the sequences recovered from the community in the adjacent water column belonged to the class Alphaproteobacteria. Altogether, 21 monophyletic sequence clusters, comprising sequences from both sponge adults and embryos but not from the seawater, were identified. More than half of the sponge-derived sequences fell into these clusters. Comparison of sequences recovered in this study with those deposited in GenBank revealed that more than 75% of S. zeai-derived sequences were closely related to sequences derived from other sponge species, but none of the sequences recovered from the seawater column overlapped with those from adults or embryos of S. zeai. In conclusion, there is strong evidence that a dominant proportion of sponge-specific bacteria present in the tissues of S. zeai are maintained through vertical transfer during embryogenesis rather than through acquisition from the environment (horizontal transfer).Besides being the oldest metazoans, sponges are the simplest multicellular animals and possess a low degree of tissue differentiation and coordination (54). Sponges are sessile, filter-feeding organisms that may harbor within their tissues a remarkable array of microorganisms, including bacteria (19, 59, 64), archaea (41), zooxanthellae (22), diatoms (63), and fungi (35). In some cases, microbial consortia can make up to 40 to 60% of the sponge tissue volume (21, 61) and exceed a density of 10 9 microbial cells per ml of sponge tissue (62), which is several orders of magnitude higher than that found in seawater. Apart from being a source of food (43), bacterial symbionts may participate in the acquisition and transfer of nutrients inside sponges (67, 68), the recycling of insoluble protein (69), the sta...

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Sexual reproduction in four Caribbean commercial sponges. II. Oogenesis and transfer of bacterial symbionts

Cited by 55 publications

References 10 publications

Molecular Microbial Diversity Survey of Sponge Reproductive Stages and Mechanistic Insights into Vertical Transmission of Microbial Symbionts

Molecular Microbial Diversity Survey of Sponge Reproductive Stages and Mechanistic Insights into Vertical Transmission of Microbial Symbionts

Sponge-Associated Microorganisms: Evolution, Ecology, and Biotechnological Potential

Evidence for Vertical Transmission of Bacterial Symbionts from Adult to Embryo in the Caribbean SpongeSvenzea zeai

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