Transmission of the sponge microbiome: moving towards a unified model

Oliveira, Bruno Francesco Rodrigues de; Freitas-Silva, Jéssyca; Sánchez-Robinet, Claudia; Laport, Marinella Silva

doi:10.1111/1758-2229.12896

Cited by 23 publications

(20 citation statements)

References 154 publications

(248 reference statements)

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“…In contrast, we found a higher degree of variation in some particular individuals, a situation that was previously reported in a comparison of samples from Deception Island ( Sacristán-Soriano et al, 2020 ). The stability of less complex microbiomes and the capacity of the sponge holobiont to select microorganisms from the environment in its benefit under stressing conditions ( Oliveira et al, 2020 ) could be essential in such an extreme environment. In this regard, the high stability in the microbiome of M. acerata together with high growth rates ( Dayton et al, 1974 ) might play a key role for the success of this species in colonising Antarctic benthos.…”

Section: Discussionmentioning

confidence: 99%

Stability of the Microbiome of the Sponge Mycale (Oxymycale) acerata in the Western Antarctic Peninsula

et al. 2022

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The sponge microbiome, especially in Low Microbial Abundance (LMA) species, is expected to be influenced by the local environment; however, contrasting results exist with evidence showing that host specificity is also important, hence suggesting that the microbiome is influenced by host-specific and environmental factors. Despite sponges being important members of Southern Ocean benthic communities, their relationships with the microbial communities they host remain poorly studied. Here, we studied the spatial and temporal patterns of the microbiota associated with the ecologically important LMA sponge M. acerata at sites along ∼400 km of the Western Antarctic Peninsula (WAP) to assess patterns in the core and variable microbial components of the symbiont communities of this sponge species. The analyses of 31 samples revealed that the microbiome of M. acerata is composed of 35 prokaryotic phyla (3 Archaea, 31 Bacteria, and one unaffiliated), being mainly dominated by Proteobacteria with Gammaproteobacteria as the most dominant class. The core community was composed of six prokaryotic OTUs, with gammaproteobacterial OTU (EC94 Family), showing a mean abundance over 65% of the total abundance. Despite some differences in rare OTUs, the core community did not show clear patterns in diversity and abundance associated with specific sites/environmental conditions, confirming a low variability in community structure of this species along the WAP. The analysis at small scale (Doumer Island, Palmer Archipelago) showed no differences in space and time in the microbiome M. acerata collected at sites around the island, sampled in three consecutive years (2016–2018). Our results highlight the existence of a low spatial and temporal variability in the microbiome of M. acerata, supporting previous suggestions based on limited studies on this and other Antarctic sponges.

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Section: Discussionmentioning

confidence: 99%

Stability of the Microbiome of the Sponge Mycale (Oxymycale) acerata in the Western Antarctic Peninsula

et al. 2022

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“…What are the advantages of horizontal transmission of microbiota? Since some of the microbiome members are not vertically transmitted in a reliable way [218], strong natural selection would favor hosts that can seize useful symbionts from the local environment [219,220]. Another advantage of acquiring microbes from the environment is the possibility of genetic variation and evolution of holobionts by the occasional acquisition of a novel beneficial strain [221].…”

Section: Horizontal Transmissionmentioning

confidence: 99%

“…The observation of horizontal transmission being more abundant in the marine than in terrestrial environment could arise from the simple fact that water is a conducive medium in which desiccation and osmolarity do not represent a problem, thus encouraging horizontal transmission and host to-host transfer events [4]. For example, in the sponge, Plakina cyanorosea, harboring a relatively low microbial abundance, transmission of its microbiome relies primarily, but not exclusively, on horizontal transmission [220]. However, there is now also evidence for maternal vertical inheritance in deep-sea animals as well [220,228,229], indicating a mixed vertical and horizontal transmission.…”

Section: Mixed Vertical and Horizontal Transmissionmentioning

confidence: 99%

“…For example, in the sponge, Plakina cyanorosea, harboring a relatively low microbial abundance, transmission of its microbiome relies primarily, but not exclusively, on horizontal transmission [220]. However, there is now also evidence for maternal vertical inheritance in deep-sea animals as well [220,228,229], indicating a mixed vertical and horizontal transmission. In chemosynthetic symbionts in deep-sea mussels both horizontal [230] and vertical transmission [231] have been reported.…”

Section: Mixed Vertical and Horizontal Transmissionmentioning

confidence: 99%

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Reconstitution and Transmission of Gut Microbiomes and Their Genes between Generations

Rosenberg

Zilber‐Rosenberg

2021

Microorganisms

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Microbiomes are transmitted between generations by a variety of different vertical and/or horizontal modes, including vegetative reproduction (vertical), via female germ cells (vertical), coprophagy and regurgitation (vertical and horizontal), physical contact starting at birth (vertical and horizontal), breast-feeding (vertical), and via the environment (horizontal). Analyses of vertical transmission can result in false negatives (failure to detect rare microbes) and false positives (strain variants). In humans, offspring receive most of their initial gut microbiota vertically from mothers during birth, via breast-feeding and close contact. Horizontal transmission is common in marine organisms and involves selectivity in determining which environmental microbes can colonize the organism’s microbiome. The following arguments are put forth concerning accurate microbial transmission: First, the transmission may be of functions, not necessarily of species; second, horizontal transmission may be as accurate as vertical transmission; third, detection techniques may fail to detect rare microbes; lastly, microbiomes develop and reach maturity with their hosts. In spite of the great variation in means of transmission discussed in this paper, microbiomes and their functions are transferred from one generation of holobionts to the next with fidelity. This provides a strong basis for each holobiont to be considered a unique biological entity and a level of selection in evolution, largely maintaining the uniqueness of the entity and conserving the species from one generation to the next.

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“…However, the question has been how these sponges select and obtain many of their symbionts. Three models have been proposed in microbial acquisition: (1) vertical transmission, (2) horizontal transmission, and (3) leaky vertical transmission or mixed mode of transmission, which utilizes a combination of vertical and horizontal transmission (Schmitt et al, 2008;de Oliveira et al, 2020). Vertical transmission describes the microbial acquisition primarily from parent to progeny, horizontal transmission acquires their microbiome from the environment, whereas leaky vertical transmission acquires their microbial community from both their parent and environment.…”

Section: Introductionmentioning

confidence: 99%

Characterization of Prodiginine Pathway in Marine Sponge-Associated Pseudoalteromonas sp. PPB1 in Hilo, Hawai‘i

Sakai-Kawada

Hagiwara

et al. 2020

Front. Sustain. Food Syst.

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Interest in bioactive pigments stems from their ecological role in adaptation, as well as their applications in various consumer products. The production of these bioactive pigments can be from a variety of biological sources, including simple microorganisms that may or may not be associated with a host. This study is particularly interested in the marine sponges, which have been known to harbor microorganisms that produce secondary metabolites like bioactive pigments. In this study, marine sponge tissue samples were collected from Puhi Bay off the Eastern shore of Hilo, Hawai‘i and subsequently were identified as Petrosia sp. with red pigmentation. Using surface sterilization and aseptic plating of sponge tissue samples, sponge-associated microorganisms were isolated. One isolate (PPB1) produced a colony with red pigmentation like that of Petrosia sp., suggesting an integral relationship between this particular isolate and the sponge of interest. 16S characterization and sequencing of PPB1 revealed that it belonged to the Pseudoalteromonas genus. Using various biological assays, both antimicrobial and antioxidant bioactivity was shown in Pseudoalteromonas sp. PPB1 crude extract. To further investigate the genetics of pigment production, a draft genome of PPB1 was sequenced, assembled, and annotated. This revealed a prodiginine biosynthetic pathway and the first cited-incidence of a prodiginine-producing Pseudoalteromonas species isolated from a marine sponge host. Further understanding into the bioactivity and biosynthesis of secondary metabolites like pigmented prodiginine may uncover the complex ecological interactions between host sponge and microorganism.

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Transmission of the sponge microbiome: moving towards a unified model

Cited by 23 publications

References 154 publications

Stability of the Microbiome of the Sponge Mycale (Oxymycale) acerata in the Western Antarctic Peninsula

Stability of the Microbiome of the Sponge Mycale (Oxymycale) acerata in the Western Antarctic Peninsula

Reconstitution and Transmission of Gut Microbiomes and Their Genes between Generations

Characterization of Prodiginine Pathway in Marine Sponge-Associated Pseudoalteromonas sp. PPB1 in Hilo, Hawai‘i

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