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Molecular detection and microbiome differentiation of two cryptic lineages of giant barrel sponges from Conch Reef, Florida Keys

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James S. Evans
James S. Evans
James S. Evans
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Susanna López-Legentil
Susanna López-Legentil
Susanna López-Legentil
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Joseph R Pawlik at University of North Carolina at Wilmington
Joseph R Pawlik
Isobel Turnbull at University of Plymouth
Isobel Turnbull
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Abstract and Figures

The giant barrel sponge, Xestospongia muta, represents a dominant member of Caribbean reef communities. Recent microsatellite data have revealed the presence of two genetic clusters of X. muta in a monitored population on Conch Reef, Florida Keys, with a reduced abundance of one cluster among the largest individuals. Tracking changes to populations over time and their ecological significance requires rapid identification of each genetic cluster and subsequent studies of biological differences between clusters. Here, we show that single-gene barcoding detected the same intraspecific genetic variation within X. muta from Conch Reef as microsatellite data, with mitochondrial gene sequences (cytochrome c oxidase subunit I, I3-M11 partition) from 54 individuals corresponding to 4 known haplotypes within the two genetic clusters. Remarkably, mapping these haplotypes to barrel sponges worldwide revealed positioning on opposite ends of a global network, despite their sympatric occurrence. Further, we investigated whether differences in symbiotic microbial communities could be detected between the two clusters using next-generation (Illumina) sequencing of 16S rRNA gene amplicons. Both clusters exhibited highly diverse microbial communities, with 12,185 total OTUs spanning 38 bacterial and 3 archaeal phyla, but significant differences in microbial community structure (PERMANOVA; p < 0.001) and diversity (Shannon diversity index; p < 0.01) were detected between the two clusters. As sponges typically exhibit interspecific, but not intraspecific, variability in microbial communities, these findings within a sympatric population provide additional support for ecologically relevant cryptic species of X. muta.
Venn diagram showing OTU overlap in microbial communities of Xestospongia muta genetic clusters 1 (green) and 2 (red), and in seawater (blue). Total richness among all three sources was 13,082 OTUs
Venn diagram showing OTU overlap in microbial communities of Xestospongia muta genetic clusters 1 (green) and 2 (red), and in seawater (blue). Total richness among all three sources was 13,082 OTUs
… 
Microbial community composition averaged for the three sources: Xestospongia muta genetic clusters 1 and 2, and seawater. Phylum-level classifications are shown except for Proteobacteria, which are divided into major classes (Alpha-, Delta-, and Gammaproteobacteria). “Other taxa” represents less abundant taxa and includes: AncK6, unclassified archaea, Asgardaeota, unclassified bacteria, Calditrichaeota, Chlamydiae, Crenarchaeota, Dadabacteria, Deinococcus-Thermus, Dependentiae, Elusimicrobia, Entotheonellaeota, Epsilonbacteraeota, FCPU426, Fibrobacteres, Firmicutes, Fusobacteria, Kiritimatiellaeota, Latescibacteria, LCP-89, Lentisphaerae, Margulisbacteria, Marinimicrobia (SAR406_clade), Modulibacteria, Nanoarchaeaeota, Nitrospinae, Omnitrophicaeota, Patescibacteria, Planctomycetes, unclassified Proteobacteria, Schekmanbacteria, Spirochaetes, Tenericutes, Verrucomicrobia, and Zixibacteria
Microbial community composition averaged for the three sources: Xestospongia muta genetic clusters 1 and 2, and seawater. Phylum-level classifications are shown except for Proteobacteria, which are divided into major classes (Alpha-, Delta-, and Gammaproteobacteria). “Other taxa” represents less abundant taxa and includes: AncK6, unclassified archaea, Asgardaeota, unclassified bacteria, Calditrichaeota, Chlamydiae, Crenarchaeota, Dadabacteria, Deinococcus-Thermus, Dependentiae, Elusimicrobia, Entotheonellaeota, Epsilonbacteraeota, FCPU426, Fibrobacteres, Firmicutes, Fusobacteria, Kiritimatiellaeota, Latescibacteria, LCP-89, Lentisphaerae, Margulisbacteria, Marinimicrobia (SAR406_clade), Modulibacteria, Nanoarchaeaeota, Nitrospinae, Omnitrophicaeota, Patescibacteria, Planctomycetes, unclassified Proteobacteria, Schekmanbacteria, Spirochaetes, Tenericutes, Verrucomicrobia, and Zixibacteria
… 
Non-metric multi-dimensional scaling plot based on Bray–Curtis similarity matrices of microbial communities in Xestospongia muta genetic clusters 1 (green triangles) and 2 (red triangles). The spatial grouping of all replicate samples by genetic cluster indicates a high degree of host specificity and distinct structural divisions between Cluster 1 and Cluster 2 microbial communities
Non-metric multi-dimensional scaling plot based on Bray–Curtis similarity matrices of microbial communities in Xestospongia muta genetic clusters 1 (green triangles) and 2 (red triangles). The spatial grouping of all replicate samples by genetic cluster indicates a high degree of host specificity and distinct structural divisions between Cluster 1 and Cluster 2 microbial communities
… 
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REPORT
Molecular detection and microbiome differentiation of two cryptic
lineages of giant barrel sponges from Conch Reef, Florida Keys
James S. Evans
1
•Susanna Lo
´pez-Legentil
1
•Joseph R. Pawlik
1
•Isobel G. Turnbull
2
•
Patrick M. Erwin
1
Received: 9 December 2020 / Accepted: 23 March 2021 / Published online: 30 March 2021
ÓSpringer-Verlag GmbH Germany, part of Springer Nature 2021
Abstract The giant barrel sponge, Xestospongia muta,
represents a dominant member of Caribbean reef commu-
nities. Recent microsatellite data have revealed the pres-
ence of two genetic clusters of X. muta in a monitored
population on Conch Reef, Florida Keys, with a reduced
abundance of one cluster among the largest individuals.
Tracking changes to populations over time and their eco-
logical significance requires rapid identification of each
genetic cluster and subsequent studies of biological dif-
ferences between clusters. Here, we show that single-gene
barcoding detected the same intraspecific genetic variation
within X. muta from Conch Reef as microsatellite data,
with mitochondrial gene sequences (cytochrome c oxidase
subunit I, I3-M11 partition) from 54 individuals corre-
sponding to 4 known haplotypes within the two genetic
clusters. Remarkably, mapping these haplotypes to barrel
sponges worldwide revealed positioning on opposite ends
of a global network, despite their sympatric occurrence.
Further, we investigated whether differences in symbiotic
microbial communities could be detected between the two
clusters using next-generation (Illumina) sequencing of
16S rRNA gene amplicons. Both clusters exhibited highly
diverse microbial communities, with 12,185 total OTUs
spanning 38 bacterial and 3 archaeal phyla, but significant
differences in microbial community structure (PERMA-
NOVA; p\0.001) and diversity (Shannon diversity index;
p\0.01) were detected between the two clusters. As
sponges typically exhibit interspecific, but not intraspecific,
variability in microbial communities, these findings within
a sympatric population provide additional support for
ecologically relevant cryptic species of X. muta.
Keywords Xestospongia muta Microbial symbionts
Giant barrel sponge Cryptic lineages Sponge ecology
Microbial ecology
Introduction
Coral reefs represent complex ecological systems, with
biodiversity rivaling or surpassing even that of tropical
rainforests. Sponges are particularly abundant on Car-
ibbean reefs (Loh and Pawlik 2014), with species richness
outnumbering even corals and algae (Diaz and Ru
¨tzler
2001). As spatial competitors with corals, rapid coral
decline has led to concurrent increases in sponge cover on
some reefs as sponges colonize newly available space
faster than corals (Aronson et al. 2002; McMurray et al.
2010; Bell et al. 2013; Marlow et al. 2019). In the long
term, this trend may lead to sponge-dominated reefs
replacing coral-dominated reefs (Bell et al. 2013), although
this shift will ultimately depend on the causes of coral
decline, as sponges may be similarly sensitive to environ-
mental stressors (Powell et al. 2014; reviewed in Pawlik
and McMurray 2020).
The increasing abundance of sponges on tropical reefs
may amplify the important ecological services these
Topic Editor Carly Kenkel
Supplementary Information The online version contains
supplementary material available at https://doi.org/10.1007/s00338-
021-02089-8.
&Patrick M. Erwin
erwinp@uncw.edu
1
Department of Biology & Marine Biology, Center for Marine
Science, University of North Carolina Wilmington, 5600
Marvin K. Moss Lane, Wilmington, NC 28409, USA
2
Ocean and Earth Sciences, University of Southampton,
European Way, Southampton SO14 3ZH, UK
123
Coral Reefs (2021) 40:853–865
https://doi.org/10.1007/s00338-021-02089-8
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Ascertaining how microbes influence host diversification first requires a better understanding of how microbial composition and function reflects intraspecific variation in hosts (e.g. morphological, genetic and geographical ;Evans et al., 2021;Kelly et al., 2021;Lange et al., 2023). ...
... However, the relative impacts of genetics, geography and sponge morphology on variation in microbiome composition and function is unclear, an issue further compounded by both cryptic species and phenotypically plastic forms across sponges. Microbial community differentiation between morphologically cryptic sponge lineages (Chambers et al., 2013;Cuvelier et al., 2014;Evans et al., 2021;Gloeckner et al., 2013) raises the hypothesis that symbiotic communities could mediate incipient ecological divergence and suggests that functional ecological differences could underlie hosts with distinct growth forms (Kelly et al., 2021). The pervasiveness of crypsis and phenotypic plasticity among sponges requires adequate geographical and morphological sampling of a species complex in order to examine the interplay between genetic, geographical, microbial community and function, and host phenotype. ...
... In either case, observations described here are consistent with expectations of highly differentiated populations of co-diverging holobionts (Moran & Sloan, 2015). In A. citrina and A. sceptrum, co-divergence is further supported by a significant relationship between microbiome divergence and genetic divergence ( Figure S4), similarly observed in Xestospongia muta (Evans et al., 2021), Ircinia campana (Griffiths et al., 2019) and Cliona delitrix . ...
Phylosymbiosis and metabolomics resolve phenotypically plastic and cryptic sponge species in the genus Agelas across the Caribbean basin
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Fundamental to holobiont biology is recognising how variation in microbial composition and function relates to host phenotypic variation. Sponges often exhibit considerable phenotypic plasticity and also harbour dense microbial communities that function to protect and nourish hosts. One of the most prominent sponge genera on Caribbean coral reefs is Agelas . Using a comprehensive set of morphological (growth form, spicule), chemical and molecular data on 13 recognised species of Agelas in the Caribbean basin, we were able to define only five species (=clades) and found that many morphospecies designations were incongruent with phylogenomic and population genetic analyses. Microbial communities were also strongly differentiated between phylogenetic species, showing little evidence of cryptic divergence and relatively low correlation with morphospecies assignment. Metagenomic analyses also showed strong correspondence to phylogenetic species, and to a lesser extent, geographical and morphological characters. Surprisingly, the variation in secondary metabolites produced by sponge holobionts was explained by geography and morphospecies assignment, in addition to phylogenetic species, and covaried significantly with a subset of microbial symbionts. Spicule characteristics were highly plastic, under greater impact from geographical location than phylogeny. Our results suggest that while phenotypic plasticity is rampant in Agelas , morphological differences within phylogenetic species affect functionally important ecological traits, including the composition of the symbiotic microbial communities and metabolomic profiles.
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... Until recently, the most abundant species of the genus Xestospongia were identified as X. muta in the Caribbean and X. testudinaria in the Indo-Pacific. However, recent genetic studies documented that these different Xestospongia species are part of a more diverse species complex (Evans et al., 2021;Swierts et al., 2017). Morphologically similar species occur sympatrically and might feature differences in their physiology. ...
... Although three species of Xestospongia, namely X. muta, X. testudinaria, and X. bergquistia, are recognized globally, recent studies suggest that these species are part of complexes consisting of cryptic species (Evans et al., 2021;Swierts et al., 2017). Swierts et al. (2017) analyzed 10 Xestospongia samples from Koh Tao (only~40 km away from our sampling sites) and identified three different haplotypes. ...
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Marine sponges are prominent organisms of the benthic coral reef fauna, providing important ecosystem services. While there have been increasing reports that sponges are becoming one of the dominant benthic organisms in some locations and ecoregions (e.g. Caribbean), they can be impacted by changing environmental conditions. This study presents the first documentation of a mass mortality event of the barrel sponge Xestospongia sp. in the lower Gulf of Thailand and its consequences on population dynamics and size distribution. Two anthropogenic impacted reefs (Haad Khom and Mae Haad) of the island Koh Phangan and two anthropogenic non-impacted reefs of the islands Koh Yippon and Hin Yippon within the Mu Ko Ang Thong Marine National Park were surveyed in the years 2015 and 2016. The results showed a strong shift in population densities at Koh Phangan. Fatal "bleaching" ending up in mass mortality was observed for these reefs in 2015. Xestospongia sp. abundance decreased from 2015 to 2016 by 80.6% at Haad Khom and by 98.4% at Mae Haad. Sponges of all sizes were affected, and mortality occurred regardless of the survey depth (4 and 6 m). However, Xestospongia population densities in the Marine Park were at a constant level during the surveys. The abundances in 2015 were 65% higher at the Marine Park than at Koh Phangan and 92% higher in 2016. The most likely causes of the mass mortality event was a local harmful algal bloom event, pathogens, undetected local higher water temperatures, or a combination of these factors, whereas sea surface temperature analyses showed no marine heatwave during the observed mass mortality event in 2015. Considering the ecological importance of sponges such as Xestospongia sp., long-term monitoring of reefs and their environmental parameters should be implemented to prevent such mass die-offs.
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... Sponges possess diverse and highly species-specific microbiomes (Taylor et al. 2007;Lee et al. 2011;Schmitt et al. 2012;Thomas et al. 2016); however, intraspecific differences can result from geographic separation (Fiore et al 2013b;Marino et al. 2017) and genetic differences (Griffiths et al. 2019;Díez-Vives et al. 2020;Easson et al. 2020). Indeed, within the Caribbean giant barrel sponges, microbiome differentiation has been detected among sympatric individuals (Evans et al. 2021) consistent with the species boundaries proposed by Swierts et al. (2017). Demographic analyses of the same population revealed a shift in the dominant genetic group (Deignan et al. 2018), which when coupled with the microbiome data, suggests that there may also be a shift in ecological functioning or niche partitioning occurring for these important reef inhabitants. ...
... We recommend additional studies with increased sampling effort to include sufficient replication of all haplotypes within each geographic region to conclusively confirm the results reported here. Additionally, research coupling demographic surveys of X. testudinaria within Singapore with their genetic composition is required to determine if the barrel sponges are experiencing similar shifts in genetic structure as observed in the Caribbean (Deignan et al. 2018;Evans et al. 2021). These results highlight the usefulness of merging microbiome and molecular data in assigning species boundaries and hint at potential functional differences that allow the sponges to coexist sympatrically. ...
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... Is there a genetic difference between the morphotypes? GBSs were recently found to include several cryptic species [11][12][13], with evidence of genetic differentiation among sponges with different surface morphologies on reefs off the coast of Indonesia [5]. We sequenced a fragment of the barcoding gene (mtDNA-COI) on tissue samples from six sponges each with the clam and normal barrel morphotypes from Barbados and compared these with samples of normal barrel morphotypes from a long-term study of GBSs on Conch Reef, Florida Keys [12,14] and the global network of GBS haplotype diversity [11,13] (Table 1). ...
... GBSs were recently found to include several cryptic species [11][12][13], with evidence of genetic differentiation among sponges with different surface morphologies on reefs off the coast of Indonesia [5]. We sequenced a fragment of the barcoding gene (mtDNA-COI) on tissue samples from six sponges each with the clam and normal barrel morphotypes from Barbados and compared these with samples of normal barrel morphotypes from a long-term study of GBSs on Conch Reef, Florida Keys [12,14] and the global network of GBS haplotype diversity [11,13] (Table 1). While the sponges with the clam morphotype shared the same haplotype (C2/H1), they also shared this haplotype with sponges having the normal barrel morphotype from Barbados, other locations in the Caribbean Sea, and other ocean basins (Table 1). ...
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... Bioremediasi logam berat oleh bakteri didasarkan pada penjenuhan kutub-kutub negatif permukaan bakteri oleh ion positif yang dimiliki oleh logam berat, sehingga jika terjadi kondisi yang sesuai maka akan terjadi pengikatan kompleks logam berat oleh bakteri. Reaksi ini berakibat terjadinya kejenuhan bakteri menjerap ion positif logam berat (Evans et al., 2021). Tabel 9.3, menyajikan beberapa jenis bakteri yang mampu meremediasi limbah organik dan anorganik. ...
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... 357,3 nm. The determination of the absorption of each test pollutant must fall within the range of the calibration curve that has been made for each test metal pollutant to see the bioremediation performance of the two types of sponge symbiont bacteria as bio-adsorbents against Mercury and Nickel ion pollutants [34], [35]. Experimental bioremediation of AF and AC bacteria is briefly presented in the schematic. ...
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Full-text available
  • Oct 2017
Four mesophilic, neutrophilic, and aerobic marine ammonia-oxidizing archaea, designated strains SCM1(T), HCA1(T), HCE1(T) and PS0(T), were isolated from a tropical marine fish tank, dimly lit deep coastal waters, the lower euphotic zone of coastal waters, and near-surface sediment in the Puget Sound estuary, respectively. Cells are straight or slightly curved small rods, 0.15-0.26 µm in diameter and 0.50-1.59 µm in length. Motility was not observed, although strain PS0(T) possesses genes associated with archaeal flagella and chemotaxis, suggesting it may be motile under some conditions. Cell membranes consist of glycerol dibiphytanyl glycerol tetraether (GDGT) lipids, with crenarchaeol as the major component. Strain SCM1(T) displays a single surface layer (S-layer) with p6 symmetry, distinct from the p3-S-layer reported for the soil ammonia-oxidizing archaeon Nitrososphaera viennensis EN76(T). Respiratory quinones consist of fully saturated and monounsaturated menaquinones with 6 isoprenoid units in the side chain. Cells obtain energy from ammonia oxidation and use carbon dioxide as carbon source; addition of an α-keto acid (α-ketoglutaric acid) was necessary to sustain growth of strains HCA1(T), HCE1(T), and PS0(T). Strain PS0(T) uses urea as a source of ammonia for energy production and growth. All strains synthesize vitamin B1 (thiamine), B2 (riboflavin), B6 (pyridoxine), and B12 (cobalamin). Optimal growth occurs between 25 and 32 °C, between pH 6.8 and 7.3, and between 25 and 37 ‰ salinity. All strains have a low mol% G+C content of 33.0-34.2. Strains are related by 98 % or greater 16S rRNA gene sequence identity, sharing ~85 % 16S rRNA gene sequence identity with Nitrososphaera viennensis EN76(T). All four isolates are well separated by phenotypic and genotypic characteristics and are here assigned to distinct species within the genus Nitrosopumilus gen. nov. Isolates SCM1(T) (=ATCC TSD-97(T) =NCIMB 15022(T)), HCA1(T) (=ATCC TSD-96(T)), HCE1(T) (=ATCC TSD-98(T)), and PS0(T) (=ATCC TSD-99(T)) are type strains of the species Nitrosopumilusmaritimus sp. nov., Nitrosopumilus cobalaminigenes sp. nov., Nitrosopumilus oxyclinae sp. nov., and Nitrosopumilus ureiphilus sp. nov., respectively. In addition, we propose the family Nitrosopumilaceae fam. nov. and the order Nitrosopumilales ord. nov. within the class Nitrososphaeria.
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Globally intertwined evolutionary history of giant barrel sponges
Article
Full-text available
  • Sep 2017
  • CORAL REEFS
p>Three species of giant barrel sponge are currently recognized in two distinct geographic regions, the tropical Atlantic and the Indo-Pacific. In this study, we used molecular techniques to study populations of giant barrel sponges across the globe and assessed whether the genetic structure of these populations agreed with current taxonomic consensus or, in contrast, whether there was evidence of cryptic species. Using molecular data, we assessed whether giant barrel sponges in each oceanic realm represented separate monophyletic lineages. Giant barrel sponges from 17 coral reef systems across the globe were sequenced for mitochondrial (partial CO1 and ATP6 genes) and nuclear (ATPsβ intron) DNA markers. In total, we obtained 395 combined sequences of the mitochondrial CO1 and ATP6 markers, which resulted in 17 different haplotypes. We compared a phylogenetic tree constructed from 285 alleles of the nuclear intron ATPsβ to the 17 mitochondrial haplotypes. Congruent patterns between mitochondrial and nuclear gene trees of giant barrel sponges provided evidence for the existence of multiple reproductively isolated species, particularly where they occurred in sympatry. The species complexes in the tropical Atlantic and the Indo-Pacific, however, do not form separate monophyletic lineages. This rules out the scenario that one species of giant barrel sponge developed into separate species complexes following geographic separation and instead suggests that multiple species of giant barrel sponges already existed prior to the physical separation of the Indo-Pacific and tropical Atlantic.</p
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The Emerging Ecological and Biogeochemical Importance of Sponges on Coral Reefs
Article
  • Jan 2020
With the decline of reef-building corals on tropical reefs, sponges have emerged as an important component of changing coral reef ecosystems. Seemingly simple, sponges are highly diverse taxonomically, morphologically, and in terms of their relationships with symbiotic microbes, and they are one of nature's richest sources of novel secondary metabolites. Unlike most other benthic organisms, sponges have the capacity to disrupt boundary flow as they pump large volumes of seawater into the water column. This seawater is chemically transformed as it passes through the sponge body as a consequence of sponge feeding, excretion, and the activities of microbial symbionts, with important effects on carbon and nutrient cycling and on the organisms in the water column and on the adjacent reef. In this review, we critically evaluate developments in the recently dynamic research area of sponge ecology on tropical reefs and provide a perspective for future studies. Expected final online publication date for the Annual Review of Marine Science Volume 12 is January 3, 2020. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
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Social transitions in sponge-dwelling snapping shrimp
Article
  • Mar 2019
Sociality is exceedingly rare in the marine environment, with true eusociality found only within a single genus of sponge-dwelling snapping shrimp. This genus is socially diverse and exhibits multiple independent evolutionary origins of both eusociality and communal breeding from pair-forming ancestors. Ecology was critical to the evolution of shrimp sociality, as the transition from host specialization to generalism preceded the evolution of eusociality, and the transition from small to large host sponges favored the evolution of communal breeding. Moreover, a change in life history from planktonic to non-dispersing, crawling larvae only occurred in eusocial species. Here, we present a hypothesis describing the evolutionary transitions toward sociality in shrimp that serves to illustrate how ecology and life history interact to shape social evolution more broadly.
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Bioeroding sponge assemblages: the importance of substrate availability and sediment
Article
  • Mar 2018
Despite global deterioration of coral reef health, not all reef-associated organisms are in decline. Bioeroding sponges are thought to be largely resistant to the factors that stress and kill corals, and are increasing in abundance on many reefs. However, there is a paucity of information on how environmental factors influence spatial variation in the distribution of these sponges, and how they might be affected by different stressors. We aimed to identify the factors that explained differences in bioeroding sponge abundance and assemblage composition, and to determine whether bioeroding sponges benefit from the same environmental conditions that can contribute towards coral mortality. Abundance surveys were conducted in the Wakatobi region of Indonesia on reefs characterized by different biotic and abiotic conditions. Bioeroding sponges occupied an average of 8.9% of available dead substrate and variation in abundance and assemblage composition was primarily attributed to differences in the availability of dead substrate. Our results imply that if dead substrate availability increases as a consequence of coral mortality, bioeroding sponge abundance is also likely to increase. However, bioeroding sponge abundance was lowest on a sedimented reef, despite abundant dead substrate. This suggests that not all forms of coral mortality will benefit all bioeroding sponge species, and sediment-degraded reefs are likely to be dominated by a few resilient bioeroding sponge species. Overall, we demonstrate the importance of understanding the drivers of bioeroding sponge abundance and assemblage composition in order to predict possible impacts of different stressors on reefs communities.
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