Maternal provisioning of an obligate symbiont in a sponge

Carrier, Tyler J.; Schmittmann, Lara; Jung, Sabrina; Pita, Lucía; Hentschel, Ute

doi:10.1002/ece3.10012

Cited by 4 publications

(2 citation statements)

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“…This outcome suggests that microbial densities and taxa richness are not always correlated 62 , and highlights the relevance of the rare taxa to the overall diversity, especially in microbiota dominated by one or few symbionts (but see below) 63 . In LMA microbiomes dominated by one or few ASVs (as in C. crambe ) dominant microbes are transmitted from adults to embryos with high fidelity thanks to brooding reproduction, as these symbionts are essential for fitness 25 , 64 – 66 . Instead, background taxa are mainly acquired horizontally from the water column 63 , 67 .…”

Section: Discussionmentioning

confidence: 99%

High microbiome and metabolome diversification in coexisting sponges with different bio-ecological traits

Mazzella,

Dell’Anno,

Etxebarría

et al. 2024

Commun Biol

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Marine Porifera host diverse microbial communities, which influence host metabolism and fitness. However, functional relationships between sponge microbiomes and metabolic signatures are poorly understood. We integrate microbiome characterization, metabolomics and microbial predicted functions of four coexisting Mediterranean sponges –Petrosia ficiformis, Chondrosia reniformis, Crambe crambe and Chondrilla nucula. Microscopy observations reveal anatomical differences in microbial densities. Microbiomes exhibit strong species-specific trends. C. crambe shares many rare amplicon sequence variants (ASV) with the surrounding seawater. This suggests important inputs of microbial diversity acquired by selective horizontal acquisition. Phylum Cyanobacteria is mainly represented in C. nucula and C. crambe. According to putative functions, the microbiome of P. ficiformis and C. reniformis are functionally heterotrophic, while C. crambe and C. nucula are autotrophic. The four species display distinct metabolic profiles at single compound level. However, at molecular class level they share a “core metabolome”. Concurrently, we find global microbiome-metabolome association when considering all four sponge species. Within each species still, sets of microbe/metabolites are identified driving multi-omics congruence. Our findings suggest that diverse microbial players and metabolic profiles may promote niche diversification, but also, analogous phenotypic patterns of “symbiont evolutionary convergence” in sponge assemblages where holobionts co-exist in the same area.

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Section: Discussionmentioning

confidence: 99%

High microbiome and metabolome diversification in coexisting sponges with different bio-ecological traits

Mazzella,

Dell’Anno,

Etxebarría

et al. 2024

Commun Biol

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“…Differences in our study may arise particularly due to H. panicea , whose high archaeal diversity is responsible for a change in overall group means and differs from our initial expectations. In cases such as this, the low bacterial diversity is linked to the high abundance of a single taxon, which persists in the host and is often passed on directly to its offspring ( Schmittmann et al, 2022 ; Carrier et al, 2023 ). Variability in symbiont presence/absence and abundance can occur among different host populations but also different sampled body parts.…”

Section: Discussionmentioning

confidence: 99%

The archaeome in metaorganism research, with a focus on marine models and their bacteria–archaea interactions

von Hoyningen-Huene,

Bang,

Rausch

et al. 2024

Front. Microbiol.

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Metaorganism research contributes substantially to our understanding of the interaction between microbes and their hosts, as well as their co-evolution. Most research is currently focused on the bacterial community, while archaea often remain at the sidelines of metaorganism-related research. Here, we describe the archaeome of a total of eleven classical and emerging multicellular model organisms across the phylogenetic tree of life. To determine the microbial community composition of each host, we utilized a combination of archaea and bacteria-specific 16S rRNA gene amplicons. Members of the two prokaryotic domains were described regarding their community composition, diversity, and richness in each multicellular host. Moreover, association with specific hosts and possible interaction partners between the bacterial and archaeal communities were determined for the marine models. Our data show that the archaeome in marine hosts predominantly consists of Nitrosopumilaceae and Nanoarchaeota, which represent keystone taxa among the porifera. The presence of an archaeome in the terrestrial hosts varies substantially. With respect to abundant archaeal taxa, they harbor a higher proportion of methanoarchaea over the aquatic environment. We find that the archaeal community is much less diverse than its bacterial counterpart. Archaeal amplicon sequence variants are usually host-specific, suggesting adaptation through co-evolution with the host. While bacterial richness was higher in the aquatic than the terrestrial hosts, a significant difference in diversity and richness between these groups could not be observed in the archaeal dataset. Our data show a large proportion of unclassifiable archaeal taxa, highlighting the need for improved cultivation efforts and expanded databases.

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Dynamics, diversity, and roles of bacterial transmission modes during the first asexual life stages of the freshwater sponge Spongilla lacustris

Paix,

van der Valk,

de Voogd

2024

Environmental Microbiome

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Background Sponge-associated bacteria play important roles in the physiology of their host, whose recruitment processes are crucial to maintain symbiotic associations. However, the acquisition of bacterial communities within freshwater sponges is still under explored. Spongilla lacustris is a model sponge widely distributed in European rivers and lakes, producing dormant cysts (named gemmules) for their asexual reproduction, before winter. Through an in vitro experiment, this study aims to describe the dynamics of bacterial communities and their transmission modes following the hatching of these gemmules. Results An overall change of bacterial β-diversity was observed through the ontology of the juvenile sponges. These temporal differences were potentially linked, first to the osculum acquisition and the development of a canal system, and then, the increasing colonization of the Chlorella-like photosymbionts. Gemmules hatching with a sterilized surface were found to have a more dispersed and less diverse microbiome, revealing the importance of gemmule epibacteria for the whole holobiont stability. These epibacteria were suggested to be vertically transmitted from the maternal tissues to the gemmule surface. Vertical transmission through the incorporation of bacterial communities inside of the gemmule, was also found as a dominant transmission mode, especially with the nitrogen fixers Terasakiellaceae. Finally, we showed that almost no ASVs were shared between the free-living community and the juveniles, suggesting that horizontal recruitment is unlikely to happen during the first stages of development. However, the free-living bacteria filtered are probably used as a source of nutrients, allowing an enrichment of copiotrophic bacteria already present within its microbiome. Conclusions This study brings new insight for a better understanding of the microbiome acquisition during the first stages of freshwater sponge development. We showed the importance of epibacterial communities on gemmules for the whole holobiont stability, and demonstrated the near absence of recruitment of free-living bacteria during the first stages.

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Maternal provisioning of an obligate symbiont in a sponge

Cited by 4 publications

References 68 publications

High microbiome and metabolome diversification in coexisting sponges with different bio-ecological traits

High microbiome and metabolome diversification in coexisting sponges with different bio-ecological traits

The archaeome in metaorganism research, with a focus on marine models and their bacteria–archaea interactions

Dynamics, diversity, and roles of bacterial transmission modes during the first asexual life stages of the freshwater sponge Spongilla lacustris

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