Dynamic microbiome diversity shaping the adaptation of sponge holobionts in coastal waters DOI Creative Commons
B. C. Gan, Kai Wang, Beibei Zhang

et al.

Microbiology Spectrum, Journal Year: 2024, Volume and Issue: 12(11)

Published: Oct. 14, 2024

ABSTRACT The microbial communities associated with sponges contribute to the adaptation of hosts environments, which are essential for trophic transformation benthic-marine coupling. However, little is known about symbiotic community interactions and adaptative strategies high- low-microbial abundance (HMA LMA) sponges, represent two typical ecological phenotypes. Here, we compared 1-year dynamic patterns microbiomes HMA sponge Spongia officinalis LMA species Tedania sp. Haliclona simulans widespread on coast China. Symbiotic bacterial characteristic HMA–LMA dichotomy presented higher diversity stability in S. than H. , while archaeal showed consistent across all throughout year. Dissolved oxygen, dissolved inorganic phosphorus, organic especially temperature were major factors affecting seasonal changes communities. -associated microbiome had diversity, stronger stability, closer interaction, adopted a relatively isolated strategy cope environmental changes, more susceptible shared Amplicon Sequence Variants (ASVs) surrounding waters, an open way facing uncertainty environment. Meta-analysis composition, function from 13 marine further supported that have evolved distinct strategies. We propose different adaptive ways responding environment may be responsible their successful evolution competence global ocean change. IMPORTANCE During long-term evolution, holobionts, among oldest relationships between microbes metazoans, developed phenotypes LMA). Despite sporadic studies indicating assemblages present symbionts environments still unclear. This deficiency limits our understanding selection functions during evolutionary history assessment variable environments. explored combined meta-analysis sponges. adapting basically drawn: acclimated forming loose-connected communities, tight-connected similar beyond divergence geographical location.

Language: Английский

Symbiont transmission in marine sponges: reproduction, development, and metamorphosis DOI Creative Commons
Tyler J. Carrier, Manuel Maldonado, Lara Schmittmann

et al.

BMC Biology, Journal Year: 2022, Volume and Issue: 20(1)

Published: May 6, 2022

Abstract Marine sponges (phylum Porifera) form symbioses with diverse microbial communities that can be transmitted between generations through their developmental stages. Here, we integrate embryology and microbiology to review how symbiotic microorganisms are in this early-diverging lineage. We describe vertical transmission is widespread but not universal, microbes vertically during a select window, properties of the microbiome depends on whether species high or low abundance sponge. Reproduction, development, symbiosis thus deeply rooted, why these partnerships remains central elusive tenet symbioses.

Language: Английский

Citations

40
The source of microbial transmission influences niche colonization and microbiome development DOI

Isabel S. Tanger,

Julia Stefanschitz,

Yannick Schwert

et al.

Proceedings of the Royal Society B Biological Sciences, Journal Year: 2024, Volume and Issue: 291(2016)

Published: Feb. 6, 2024

Early life microbial colonizers shape and support the immature vertebrate immune system. Microbial colonization relies on vertical route via parental provisioning horizontal environmental contribution. Vertical transmission is mostly a maternal trait making it hard to determine source of in order gain insight into establishment community during crucial development stages. The evolution unique male pregnancy pipefishes seahorses enables disentanglement both transmission, but also facilitates differentiation versus paternal ranging from egg development, early juvenile development. Using 16S rRNA amplicon sequencing source-tracker analyses, we revealed how distinct origins (maternal, horizontal) shaped internal external microbiome broad-nosed pipefish Syngnathus typhle . Our data suggest that transovarial contribution influences gut whereas mainly shapes microbiome. identification key microbes reveals temporal shifts enhances our understanding routes, dynamics their impact lifestyle evolution.

Language: Английский

Citations

10
Global patterns in symbiont selection and transmission strategies in sponges DOI Creative Commons
Cristina Díez‐Vives, Vasiliki Koutsouveli, María Conejero

et al.

Frontiers in Ecology and Evolution, Journal Year: 2022, Volume and Issue: 10

Published: Oct. 26, 2022

Sponges host dense and diverse communities of microbes (known as the microbiome) beneficial for nutrition defense. Symbionts in turn receive shelter metabolites from sponge host, making their relationship both partners. Given that sponge-microbes associations are fundamental survival both, especially sponge, such is maintained through life even passed on to future generations. In many organisms, microbiome has profound effects development but influence reproductive developmental pathways sponges less understood. sponges, oocytes, sperm, embryos, larvae vertical transmission), using a variety methods include direct uptake mesohyl phagocytosis by oocytes indirect transmission oocyte nurse cells. Such can remain elements untouched, transfer offspring, or be digested make yolky nutrient reserves larvae. When how those decisions made fundamentally unanswered questions reproduction. Here we review diversity modes existent entire phylum Porifera detailed imaging electron microscopy, available metabarcoding data elements, macroevolutionary patterns associated phylogenetic constraints. Additionally, examine fidelity this possible reasons observed variability some stages. Our current understanding marine however, adult microbial community established combination horizontal (acquisition surrounding environment each new generation) processes, although extent which mode shapes still remains determined. We also assessed role filtration, cellular structures acquiring external microbes, immune system, ultimately stable prokaryotes sponges.

Language: Английский

Citations

23
Archaeal lipids DOI
Tomáš Řezanka, Lucie Kyselová, Denis J. Murphy

et al.

Progress in Lipid Research, Journal Year: 2023, Volume and Issue: 91, P. 101237 - 101237

Published: May 25, 2023

Language: Английский

Citations

13
Divergent morphological and microbiome strategies of two neighbor sponges to cope with low pH in Mediterranean CO2 vents DOI Creative Commons

Jana Efremova,

Valerio Mazzella, Alice Mirasole

et al.

The Science of The Total Environment, Journal Year: 2024, Volume and Issue: 916, P. 170171 - 170171

Published: Jan. 19, 2024

Ocean Acidification (OA) profoundly impacts marine biochemistry, resulting in a net loss of biodiversity. Porifera are often forecasted as winner taxa, yet the strategies to cope with OA can vary and may generate diverse fitness status. In this study, microbial shifts based on V

Language: Английский

Citations

3
From Sea to Freshwater: Shared and Unique Microbial Traits in Sponge Associated Prokaryotic Communities DOI
Michelle Guzmán de Fernandes, Gabriel Nascimento-Silva, Enrique E. Rozas

et al.

Current Microbiology, Journal Year: 2025, Volume and Issue: 82(4)

Published: March 8, 2025

Language: Английский

Citations

0
Polycystine radiolarians associate with diverse phytoplankton DOI
Nicole L. Coots, Leocadio Blanco‐Bercial, Gillian H. Gile

et al.

Journal of Plankton Research, Journal Year: 2025, Volume and Issue: 47(3)

Published: April 3, 2025

Abstract Radiolarians are marine protists with a global distribution. Epipelagic radiolarians host photosynthetic endosymbionts, but the identity and specificity of this relationship appears to vary between radiolarian subgroups. While class Acantharea order Collodaria both possess stable relatively specific relationships haptophyte Phaeocystis dinoflagellate Brandtodinium nutricula, respectively, orders Nassellaria Spumellaria (which comprise solitary Polycystinea) might have greater flexibility in terms their photosymbionts. However, little molecular data has been generated identify phytoplankton which polycystines can associate. Here, we performed short-read 16S 18S rRNA gene sequencing universal primers on single polycystine cells collected from Sargasso Sea determine common members holobiont. previous work photosymbioses suggested that they almost always exclusively associate B. determined instead associated wide diversity phytoplankton, holobiont is distinct environmental samples. Finally, found substantial proportion reads cell samples were opisthokont origin (mostly copepods), revealing other possible interactions an uncultivable difficult-to-study protist its environment.

Language: Английский

Citations

0
Microbes from Mum: symbiont transmission in the tropical reef sponge Ianthella basta DOI Creative Commons
J Pamela Engelberts, Muhammad Azmi Abdul Wahab, Manuel Maldonado

et al.

ISME Communications, Journal Year: 2022, Volume and Issue: 2(1)

Published: Sept. 27, 2022

Most marine sponge species harbour distinct communities of microorganisms which contribute to various aspects their host's health and physiology. In addition key roles in nutrient transformations chemical defence, these symbiotic microbes can shape phenotype by mediating important developmental stages influencing the environmental tolerance host. However, characterisation each microbial taxon throughout a sponge's life cycle remains challenging, with several hosting up 3000 species. Ianthella basta, an abundant broadcast spawning Indo-Pacific, is emerging model for symbiosis research as it harbours only three dominant symbionts: Thaumarchaeotum, Gammaproteobacterium, Alphaproteobacterium. Here, we successfully spawned characterised its mode reproduction, used 16S rRNA gene amplicon sequencing, fluorescence situ hybridisation, transmission electron microscopy characterise community cycle. We confirmed I. basta being gonochoric showed that symbionts, together make >90% microbiome according abundance, are vertically transmitted from mother offspring unique method involving encapsulation peri-oocytic space, suggesting obligate relationship between

Language: Английский

Citations

13
Contribution of Maternal and Paternal Transmission to Bacterial Colonization in Nematostella vectensis DOI Creative Commons
Laura Baldassarre, Shani Levy,

Rinat Bar‐Shalom

et al.

Frontiers in Microbiology, Journal Year: 2021, Volume and Issue: 12

Published: Oct. 11, 2021

Microbial communities confer multiple beneficial effects to their multicellular hosts. To evaluate the evolutionary and ecological implications of animal-microbe interactions, it is essential understand how bacterial colonization secured maintained during transition from one generation next. However, mechanisms symbiont transmission are poorly studied for many species, especially in marine environments, where surrounding water constitutes an additional source microbes. Nematostella vectensis , estuarine cnidarian, has recently emerged as model organism studies on host-microbes interactions. Here, we use this study colonizers, evaluating contribution parental environmental establishment offspring. We induced spawning adult male female polyps N. used gametes five individual fertilization experiments. While embryos developed into primary polyps, sampled each developmental stage its corresponding medium samples. By analyzing microbial community compositions all samples through 16S rRNA gene amplicon sequencing, showed that host tissues harbor microbiota significantly different medium. Interestingly, oocytes sperms associated with distinct communities, indicating specific vertical colonizers by gametes. These differences were consistent among families analyzed. overlapping identified ASVs gametes, offspring parents, well supported candidates via mothers fathers. This first investigating bacteria few spawners do not brood larvae. Our results shed light yet maternal paternal transfer symbionts along life stages generations aquatic invertebrate.

Language: Английский

Citations

18
Microbiome of the freshwater sponge Ephydatia muelleri shares compositional and functional similarities with those of marine sponges DOI Open Access
Scott Sugden, Johannes Holert, Erick Cardenas

et al.

The ISME Journal, Journal Year: 2022, Volume and Issue: 16(11), P. 2503 - 2512

Published: July 29, 2022

Language: Английский

Citations

12