Prokaryotic communities of Indo-Pacific giant barrel sponges are more strongly influenced by geography than host phylogeny

Swierts, Thomas; Cleary, Daniel F. R.; Voogd, Nicole J. de

doi:10.1093/femsec/fiy194

Cited by 33 publications

(32 citation statements)

References 86 publications

(104 reference statements)

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“…The most dominant core taxa were also observed at low abundance in the environment, while the Cliona ‐specific taxa all occurred at low abundance within the host sponge. To date, microbiome divergence has been observed at the level of host species with limited evidence of divergence among populations (Griffiths et al, ; Swierts et al, ). The results of the current study add to this body of evidence and indicate that microbiome divergence can be observed at the population genetic scale, prior to the onset of speciation.…”

Section: Discussionmentioning

confidence: 99%

Host population genetics and biogeography structure the microbiome of the sponge Cliona delitrix

Easson

Chaves‐Fonnegra

Thacker

et al. 2020

Ecology and Evolution

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Sponges occur across diverse marine biomes and host internal microbial communities that can provide critical ecological functions. While strong patterns of host specificity have been observed consistently in sponge microbiomes, the precise ecological relationships between hosts and their symbiotic microbial communities remain to be fully delineated. In the current study, we investigate the relative roles of host population genetics and biogeography in structuring the microbial communities hosted by the excavating sponge Cliona delitrix. A total of 53 samples, previously used to demarcate the population genetic structure of C. delitrix, were selected from two locations in the Caribbean Sea and from eight locations across the reefs of Florida and the Bahamas. Microbial community diversity and composition were measured using Illumina‐based high‐throughput sequencing of the 16S rRNA V4 region and related to host population structure and geographic distribution. Most operational taxonomic units (OTUs) specific to Cliona delitrix microbiomes were rare, while other OTUs were shared with congeneric hosts. Across a large regional scale (>1,000 km), geographic distance was associated with considerable variability of the sponge microbiome, suggesting a distance–decay relationship, but little impact over smaller spatial scales (<300 km) was observed. Host population structure had a moderate effect on the structure of these microbial communities, regardless of geographic distance. These results support the interplay between geographic, environmental, and host factors as forces determining the community structure of microbiomes associated with C. delitrix. Moreover, these data suggest that the mechanisms of host regulation can be observed at the population genetic scale, prior to the onset of speciation.

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Section: Discussionmentioning

confidence: 99%

Host population genetics and biogeography structure the microbiome of the sponge Cliona delitrix

Easson

Chaves‐Fonnegra

Thacker

et al. 2020

Ecology and Evolution

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“…Although the sampling sites are only approximately 70 km apart, location accounted for 12.4% of the total microbiome variation observed across samples. Microbiomes vary within species by geographic location in a number of benthic marine organisms (Pantos, Bongaerts, Dennis, Tyson, & Hoegh‐Guldberg, ; Rubio‐Portillo, Kersting, Linares, Ramos‐Esplá, & Antón, ; van de Water, Allemand, & Ferrier‐Pagès, ), including in some sponge species (Fiore et al, ; Luter et al, ; Marino et al, ; Swierts et al, ), although this finding is not universal (Pita, López‐Legentil, & Erwin, ; Pita, Turon, et al, ). Marino et al () showed a latitudinal gradient in microbiome composition in I. campana in the Caribbean, which also correlated with host mitochondrial haplotype.…”

Section: Discussionmentioning

confidence: 99%

“…Location was the largest driver of microbiome structure in this study. (Fiore et al, 2013;Luter et al, 2015;Marino et al, 2017;Swierts et al, 2018), although this finding is not universal Pita, Turon, et al, 2013). Marino et al (2017)…”

Section: Geographic Locationmentioning

confidence: 94%

“…Despite the strong effect of host species identity, significant variation in microbiome composition is still present within host sponge species (Thomas et al, 2016;Turon et al, 2018). Intraspecific microbiome variation has been associated with environmental variation, such as geographic location (Fiore, Jarett, & Lesser, 2013;Luter et al, 2015;Swierts, Cleary, & de Voogd, 2018), depth (Morrow, Fiore, & Lesser, 2016), habitat (Cleary et al, 2013;Weigel & Erwin, 2017) and water quality (Luter et al, 2015). However, given the strength of host identity in structuring the microbiome, genetic variation within the species may also be significant.…”

Section: Introductionmentioning

confidence: 99%

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Host genetics and geography influence microbiome composition in the sponge Ircinia campana

Griffiths

Antwis

Lenzi

et al. 2019

Journal of Animal Ecology

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Marine sponges are hosts to large, diverse communities of microorganisms. These microbiomes are distinct among sponge species and from seawater bacterial communities, indicating a key role of host identity in shaping its resident microbial community. However, the factors governing intraspecific microbiome variability are underexplored and may shed light on the evolutionary and ecological relationships between host and microbiome.Here, we examined the influence of genetic variation and geographic location on the composition of the Ircinia campana microbiome.We developed new microsatellite markers to genotype I. campana from two locations in the Florida Keys, USA, and characterized their microbiomes using V4 16S rRNA amplicon sequencing.We show that microbial community composition and diversity is influenced by host genotype, with more genetically similar sponges hosting more similar microbial communities. We also found that although I. campana was not genetically differentiated between sites, microbiome composition differed by location.Our results demonstrate that both host genetics and geography influence the composition of the sponge microbiome. Host genotypic influence on microbiome composition may be due to stable vertical transmission of the microbial community from parent to offspring, making microbiomes more similar by descent. Alternatively, sponge genotypic variation may reflect variation in functional traits that influence the acquisition of environmental microbes. This study reveals drivers of microbiome variation within and among locations, and shows the importance of intraspecific variability in mediating eco‐evolutionary dynamics of host‐associated microbiomes.

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“…In contrast, Luter et al (2015) found marked differences in the bacterial composition of specimens of the sponge Carteriospongia foliascens collected in the inshore Fantome and Orpheus Islands, and in Great Barrier Reef communities at Green Island and Davies Reef (Luter et al 2015). Likewise, Swierts et al (2018) found geography to be a significant determinant of prokaryotic community composition in Indo-Pacific barrel sponges (Xestospongia spp.). In order to fulfil this lack of knowledge and understand how geographical location and marine lake connectivity influence prokaryotic community composition, we assessed the prokaryotic communities of the sponge S. diversicolor Becking and Lim 2009 (Demospongiae: Hadromerida: Suberitidae) across three distinct geographical locations (Borneo, Papua and Taiwan) and two distinct marine lake habitats (relatively open and closed marine lake environments).…”

Section: Introductionmentioning

confidence: 95%

Geographical location and habitat predict variation in prokaryotic community composition of Suberites diversicolor

et al. 2020

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Purpose: Marine lakes are unique habitats that house diverse assemblages of benthic and planktonic organisms including endemic species. In this study, we aimed to assess to what extent geographical location (Berau versus Papua) and the degree of marine lake connectivity (relatively open versus closed) to the surrounding marine environment structures the prokaryotic community composition of the sponge species Suberites diversicolor. Methods: Sponge specimens were sampled in five marine lakes in Borneo and Papua and one open sea habitat in Taiwan. Result: Prokaryotic communities of S. diversicolor were dominated by members assigned to the Proteobacteria (particularly Alphaproteobacteria and Gammaproteobacteria) and Cyanobacteria, which together made up from 78 to 87% of sequences in all samples. The dominant operational taxonomic units (OTUs) in most samples, OTUs 1 and 3, were both assigned to the alphaproteobacterial order Rhodospirillales with OTU-1 dominant in the marine lakes of Berau and Papua and OTU-3 in Taiwan. OTU-3 was also largely absent from Papuan samples but present in all Berau samples. Compositionally, S. diversicolor samples clustered according to geographical location with the main axis of variation separating marine lake samples collected in Berau from those collected in Papua and the second axis of variation separating open sea samples collected in Taiwan from all marine lake samples. In addition, our results suggest that the degree of lake connectivity to the open sea also influences prokaryotic composition. Conclusion: Although previous studies have shown that sponge-associated microbial communities tend to be stable across different geographical and environmental gradients, in the present study, both geography and local environmental conditions were significant predictors of variation in prokaryotic community composition of S. diversicolor.

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Prokaryotic communities of Indo-Pacific giant barrel sponges are more strongly influenced by geography than host phylogeny

Cited by 33 publications

References 86 publications

Host population genetics and biogeography structure the microbiome of the sponge Cliona delitrix

Host population genetics and biogeography structure the microbiome of the sponge Cliona delitrix

Host genetics and geography influence microbiome composition in the sponge Ircinia campana

Geographical location and habitat predict variation in prokaryotic community composition of Suberites diversicolor

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