Communities Of Microbial Symbionts Research Articles

The impact of coral reef habitat and microbial abundance status on sponge-associated prokaryotic communities

AbstractSponges are one of the oldest lineages of animals on Earth and play key roles in shaping marine ecosystems. They are diverse, with more than 9600 species known to science, and come in a wide range of shapes, sizes, and colours. Sponges are, furthermore, known to host diverse communities of microbial symbionts, which play important roles in their physiology and ecology. In the present study, we sampled prokaryotic communities from 24 sponge species inhabiting coral reef flat and slope habitats off the coast of SW Celebes (Indonesia) in addition to sediment and seawater. The prokaryotic profiles of several sponge species were characterised for the first time. In line with previous studies, we revealed pronounced variation in diversity and composition among species with high microbial abundance (HMA) or low microbial abundance (LMA) status playing an important role in structuring prokaryotic communities across host sponge species. In addition to this, reef habitat (flat versus slope) also played a significant role in structuring prokaryotic communities. Most species in the reef slope habitat housed prokaryotic communities with a consistent profile of several cyanobacterial and prokaryotic OTUs, whereas these OTUs were largely absent from sponges inhabiting the reef flat habitat. Instead, they tended to house highly abundant bacterial populations related to the Synechococcus spongiarum group. We propose that specific strains of S. spongiarum may play a key role in enabling their host sponges to survive in an, otherwise, inhospitable environment (e.g., high irradiance and temperature) and, thus, help to explain differences in sponge composition between coral reef flat and slope habitats.

Utilizing symbiotic relationships and assisted migration in restoration to cope with multiple stressors, and the legacy of invasive species

IntroductionClimate change has increased the need for forest restoration, but low planting success and limited availability of planting materials hamper these efforts. Invasive plants and their soil legacies can further reduce restoration success. Thus, strategies that optimize restoration are crucial. Assisted migration and inoculation with native microbial symbiont communities have great potential to increase restoration success. However, assisted migrants can still show reduced survival compared to local provenances depending on transfer distance. Inoculation with mycorrhizal fungi, effective if well-matched to plants and site conditions, can have neutral to negative results with poor pairings. Few studies have examined the interaction between these two strategies in realistic field environments where native plants experience the combined effects of soil legacies left by invasive plants and the drought conditions that result from a warming, drying climate.MethodsWe planted two ecotypes (local climate and warmer climate) of Populus fremontii (Fremont cottonwoods), in soils with and without legacies of invasion by Tamarix spp. (tamarisk), and with and without addition of native mycorrhizal fungi and other soil biota from the warmer climate.ResultsFour main results emerged. 1) First year survival in soil legacies left behind after tamarisk invasion and removal was less than one tenth of survival in soil without a tamarisk legacy. 2) Actively restoring soil communities after tamarisk removal tripled first year cottonwood survival for both ecotypes, but only improved survival of the warmer, assisted migrant ecotype trees in year two. 3) Actively restoring soil communities in areas without a tamarisk history reduced first year survival for both ecotypes, but improved survival of the warmer, assisted migrant ecotype trees in year two. 4) By the second year, inoculated assisted migrants survived at five times the rate of inoculated trees from the local ecotype.DiscussionResults emphasize the detrimental effects of soil legacies left after tamarisk invasion and removal, the efficacy of assisted migration and restoring soil communities alongside plants, and the need to thoughtfully optimize pairings between plants, fungi, and site conditions.

Effects of color variation and physiological state on ascidian microbiomes.

Ascidians, known for their color variation, host species-specific microbial symbiont communities. Some ascidians can also transition into a nonfiltering (resting) physiological state. Recent studies suggest that the microbial symbiont communities may vary across different physiological states and color morphs of the host. The colonial ascidian, Polyclinum constellatum, which exhibits several color morphs in the Caribbean Sea, periodically ceases its filtering activity. To investigate if color variation in P. constellatum is indicative of sibling speciation, we sequenced fragments of the ribosomal 18S rRNA and the mitochondrial cytochrome oxidase subunit I genes. Additionally, we sequenced a fragment of the 16S rRNA gene to characterize the microbial communities of two common color morphs (red and green) in colonies that were either actively filtering (active) or nonfiltering (resting). Phylogenetic analyses of both ascidian genes resulted in well-supported monophyletic clades encompassing all color variants of P. constellatum. Interestingly, no significant differences were observed among the microbial communities of the green and red morphs, suggesting that color variation in this species is a result of intraspecific variation. However, the host's physiological state significantly influenced the microbial community structure. Nonfiltering (resting) colonies hosted higher relative abundances of Kiloniella (Alphaproteobacteria) and Fangia (Gammaproteobacteria), while filtering colonies hosted more Reugeria (Alphaproteobacteria) and Endozoicomonas (Gammaproteobacteria). This study demonstrates that microbial symbiont communities serve as reliable indicators of the taxonomic state of their host and are strongly influenced by the host's feeding condition.

Effects of sponge-to-sponge contact on the microbiomes of three spatially competing Caribbean coral reef species.

Sponges perform important ecosystem functions, host diverse microbial symbiont communities (microbiomes), and have been increasing in density on Caribbean coral reefs over the last decade. Sponges compete for space in coral reef communities through both morphological and allelopathic strategies, but no studies of microbiome impacts during these interactions have been conducted. Microbiome alterations mediate spatial competition in other coral reef invertebrates and may similarly impact competitive outcomes for sponges. In this study, we characterized the microbiomes of three common Caribbean sponges (Agelas tubulata, Iotrochota birotulata, and Xestospongia muta) observed to naturally interact spatially in Key Largo, Florida (USA). For each species, replicate samples were collected from sponges in contact with neighbors at the site of contact (contact) and distant from the site of contact (no contact), and from sponges spatially isolated from neighbors (control). Next-generation amplicon sequencing (V4 region of 16S rRNA) revealed significant differences in microbial community structure and diversity among sponge species, but no significant effects were observed within sponge species across all contact states and competitor pairings, indicating no large community shifts in response to direct contact. At a finer scale, particular symbiont taxa (operational taxonomic units at 97% sequence identity, OTUs) were shown to decrease significantly in some interaction pairings, suggesting localized effects for specific sponge competitors. Overall, these results revealed that direct contact during spatial competition does not significantly alter microbial community composition or structure of interacting sponges, suggesting that allelopathic interactions and competitive outcomes are not mediated by microbiome damage or destabilization.

Capacity of deep-sea corals to obtain nutrition from cold seeps aligned with microbiome reorganization.

Cold seeps in the deep sea harbor various animals that have adapted to utilize seepage chemicals with the aid of chemosynthetic microbes that serve as primary producers. Corals are among the animals that live near seep habitats and yet, there is a lack of evidence that corals gain benefits and/or incur costs from cold seeps. Here, we focused on Callogorgia delta and Paramuricea sp. type B3 that live near and far from visual signs of currently active seepage at five sites in the deep Gulf of Mexico. We tested whether these corals rely on chemosynthetically-derived food in seep habitats and how the proximity to cold seeps may influence; (i) coral colony traits (i.e., health status, growth rate, regrowth after sampling, and branch loss) and associated epifauna, (ii) associated microbiome, and (iii) host transcriptomes. Stable isotope data showed that many coral colonies utilized chemosynthetically derived food, but the feeding strategy differed by coral species. The microbiome composition of C. delta, unlike Paramuricea sp., varied significantly between seep and non-seep colonies and both coral species were associated with various sulfur-oxidizing bacteria (SUP05). Interestingly, the relative abundances of SUP05 varied among seep and non-seep colonies and were strongly correlated with carbon and nitrogen stable isotope values. In contrast, the proximity to cold seeps did not have a measurable effect on gene expression, colony traits, or associated epifauna in coral species. Our work provides the first evidence that some corals may gain benefits from living near cold seeps with apparently limited costs to the colonies. Cold seeps provide not only hard substrate but also food to cold-water corals. Furthermore, restructuring of the microbiome communities (particularly SUP05) is likely the key adaptive process to aid corals in utilizing seepage-derived carbon. This highlights that those deep-sea corals may upregulate particular microbial symbiont communities to cope with environmental gradients.

Microbiome of the freshwater sponge Ephydatia muelleri shares compositional and functional similarities with those of marine sponges.

Sponges are known for hosting diverse communities of microbial symbionts, but despite persistent interest in the sponge microbiome, most research has targeted marine sponges; freshwater sponges have been the focus of less than a dozen studies. Here, we used 16 S rRNA gene amplicon sequencing and shotgun metagenomics to characterize the microbiome of the freshwater sponge Ephydatia muelleri and identify potential indicators of sponge-microbe mutualism. Using samples collected from the Sooke, Nanaimo, and Cowichan Rivers on Vancouver Island, British Columbia, we show that the E. muelleri microbiome is distinct from the ambient water and adjacent biofilms and is dominated by Sediminibacterium, Comamonas, and unclassified Rhodospirillales. We also observed phylotype-level differences in sponge microbiome taxonomic composition among different rivers. These differences were not reflected in the ambient water, suggesting that other environmental or host-specific factors may drive the observed geographic variation. Shotgun metagenomes and metagenome-assembled genomes further revealed that freshwater sponge-associated bacteria share many genomic similarities with marine sponge microbiota, including an abundance of defense-related proteins (CRISPR, restriction-modification systems, and transposases) and genes for vitamin B12 production. Overall, our results provide foundational information on the composition and function of freshwater sponge-associated microbes, which represent an important yet underappreciated component of the global sponge microbiome.

Taxonomic, functional and expression analysis of viral communities associated with marine sponges.

Viruses play an essential role in shaping the structure and function of ecological communities. Marine sponges have the capacity to filter large volumes of ‘virus-laden’ seawater through their bodies and host dense communities of microbial symbionts, which are likely accessible to viral infection. However, despite the potential of sponges and their symbionts to act as viral reservoirs, little is known about the sponge-associated virome. Here we address this knowledge gap by analysing metagenomic and (meta-) transcriptomic datasets from several sponge species to determine what viruses are present and elucidate their predicted and expressed functionality. Sponges were found to carry diverse, abundant and active bacteriophages as well as eukaryotic viruses belonging to the Megavirales and Phycodnaviridae. These viruses contain and express auxiliary metabolic genes (AMGs) for photosynthesis and vitamin synthesis as well as for the production of antimicrobials and the defence against toxins. These viral AMGs can therefore contribute to the metabolic capacities of their hosts and also potentially enhance the survival of infected cells. This suggest that viruses may play a key role in regulating the abundance and activities of members of the sponge holobiont.

Microbial symbionts and ecological divergence of Caribbean sponges: A new perspective on an ancient association

Marine sponges host diverse communities of microbial symbionts that expand the metabolic capabilities of their host, but the abundance and structure of these communities is highly variable across sponge species. Specificity in these interactions may fuel host niche partitioning on crowded coral reefs by allowing individual sponge species to exploit unique sources of carbon and nitrogen, but this hypothesis is yet to be tested. Given the presence of high sponge biomass and the coexistence of diverse sponge species, the Caribbean Sea provides a unique system in which to investigate this hypothesis. To test for ecological divergence among sympatric Caribbean sponges and investigate whether these trends are mediated by microbial symbionts, we measured stable isotope (δ13C and δ15N) ratios and characterized the microbial community structure of sponge species at sites within four regions spanning a 1700 km latitudinal gradient. There was a low (median of 8.2 %) overlap in the isotopic niches of sympatric species; in addition, host identity accounted for over 75% of the dissimilarity in both δ13C and δ15N values and microbiome community structure among individual samples within a site. There was also a strong phylogenetic signal in both δ15N values and microbial community diversity across host phylogeny, as well as a correlation between microbial community structure and variation in δ13C and δ15N values across samples. Together, this evidence supports a hypothesis of strong evolutionary selection for ecological divergence across sponge lineages and suggests that this divergence is at least partially mediated by associations with microbial symbionts.

Integrative taxonomy widens our knowledge of the diversity, distribution and biology of the genus Plakina (Homosclerophorida: Plakinidae)

Despite the evolutionary significance of Homoscleromorpha, their diversity and biology are largely unknown. Here we integrate data of morphology, cytology, microbiology, ecology, reproduction, and mitochondrial cox-1 and cob gene sequences to resolve a complex of sympatric species of Plakina in South-eastern Brazil. All datasets congruently supported the delimitation of three species, two of which are new to science. Plakina coerulea has its distribution extended from one locality to over 2360 km wide. Plakina cabofriense, sp. nov. also occurs in North-eastern Brazil. Plakina cyanorosea, sp. nov. occurs only in a single, small tide pool and may be critically endangered. Plakina cyanorosea, sp. nov. produces conspicuous, abundant larvae useful for laboratory investigations. A thin, bright orange organic coat covers some spicules of P. cabofriense, sp. nov. and P. cyanorosea, sp. nov. The three Plakina species harbour diverse microbial symbiont communities, including previously unknown morphologies. Molecular phylogenies and barcoding gaps based on cox-1 and cob sequences supported that each species is monophyletic and distinct from other congeners. The genus Plakina is paraphyletic and strongly needs redefinition. The integrative approach provides new data that widens our knowledge of Homoscleromorpha diversity, distribution and biology.

Assessing the bacterial communities of sponges inhabiting the remote western Indian Ocean island of Mayotte

AbstractMarine sponges are known to host diverse and abundant communities of microbial symbionts. It has been generally assumed that the bacterial communities of low microbial abundance (LMA) sponges are less diverse than those of high microbial abundance (HMA) sponges. In this study, we used next‐generation sequencing technology to explore the bacterial communities of several biotopes including sponges, seawater, and sediment from the remote Western Indian Ocean island of Mayotte. The species investigated were the known LMA sponges: Jaspis splendens, Stylissa carteri, and Stylissa massa, and the known HMA sponges: Hyrtios erectus and Xestospongia testudinaria. In addition to this, we also investigated the following sponge species: Ectyoplasia coccinea, Paratetilla bacca, Liosina paradoxa, and Petrosia aff. spheroida of which the exact HMA/LMA status is unknown although we preliminarily classified them as HMA or LMA based on the status of closely related species. Certain HMA sponges shared similar bacterial communities dominated by Actinobacteria and Chloroflexi, whereas another species (E. coccinea) had a bacterial community closer to that of LMA sponges. Most LMA sponges housed a bacteriome dominated by Proteobacteria and Cyanobacteria, but the bacteriome of P. bacca also included dominant Chloroflexi and actinobacterial OTUs. Together with S. carteri, this sponge housed a more diverse bacterial community at the phylum, class, and order levels than HMA sponges. Although certain LMA sponges housed a bacterial community similar to the surrounding environment (seawater), they also included highly abundant, possibly species or genus specific, OTUs. Based on this study and small set of sponges studied, we conclude that a clear dichotomy between HMA and LMA sponges does not appear to exist.

Disentangling environmental and host sources of fungal endophyte communities in an experimental beachgrass study.

Disentangling the ecological factors that contribute to the assembly of the microbial symbiont communities within eukaryotic hosts is an ongoing challenge. Broadly speaking, symbiont propagules arrive either from external sources in the environment or from internal sources within the same host individual. To understand the relative importance of these propagule sources to symbiont community assembly, we characterized symbiotic fungal endophyte communities within the roots of three species of beachgrass in a field experiment. We manipulated two aspects of the external environment, successional habitat and physical disturbance. To determine the role of internal sources of propagules for endophyte community assembly, we used beachgrass individuals with different pre-existing endophyte communities. Endophyte species richness and community composition were characterized using culture-based and next-generation sequencing approaches. Our results showed that external propagule sources associated with successional habitat, but not disturbance, were particularly important for colonization of most endophytic taxa. In contrast, internal propagule sources played a minor role for most endophytic taxa but were important for colonization by the dominant taxon Microdochium bolleyi. Our findings highlight the power of manipulative field experiments to link symbiont community assembly to its underlying ecological processes, and to ultimately improve predictions of symbiont community assembly across environments.

Lipidomics of the sea sponge Amphimedon queenslandica and implication for biomarker geochemistry.

Demosponges are a rich natural source of unusual lipids, some of which are of interest as geochemical biomarkers. Although demosponges are animals, they often host dense communities of microbial symbionts, and it is therefore unclear which lipids can be synthesized by the animal de novo, and which require input from the microbial community. To address this uncertainty, we analyzed the lipids of Amphimdeon queenslandica, the only demosponge with a published genome. We correlated the genetic and lipid repertoires of A.queenslandica to identify which biomarkers could potentially be synthesized and/or modified by the sponge. The fatty acid profile of A.queenslandica is dominated by an unusual Δ5,9 fatty acid (cis-5,9-hexacosadienoic acid)-similar to what has been found in other members of the Amphimdeon genus-while the sterol profile is dominated by C27 -C29 derivatives of cholesterol. Based on our analysis of the A.queenslandica genome, we predict that this sponge can synthesize sterols de novo, but it lacks critical genes necessary to synthesize basic saturated and unsaturated fatty acids. However, it does appear to have the genes necessary to modify simpler products into a more complex "algal-like" assemblage of unsaturated fatty acids. Ultimately, our results provide additional support for the poriferan affinity of 24-isopropylcholestanes in Neoproterozoic-age rocks (the "sponge biomarker" hypothesis) and suggest that some algal proxies in the geochemical record could also have animal contributions.

Stable microbial communities in the sponge Crambe crambe from inside and outside a polluted Mediterranean harbor.

Marine sponges have been shown to harbor diverse microbial symbiont communities that play key roles in host functioning, yet little is known about how anthropogenic disturbances impact sponge-microbe interactions. The Mediterranean sponge Crambe crambe is known to accumulate heavy metals in polluted harbors. In this study, we investigated whether the microbiome of C. crambe differed between sponges inhabiting a polluted harbor in Blanes (Spain) and a nearby (<1 km) natural environment. Triplicate sponge and ambient seawater samples were collected from each site and the microbial composition of each sample was determined by 16S rRNA gene sequence analysis (Illumina Hi-Seq platform). No significant differences in the diversity or structure of microbial communities in C. crambe were detected between habitats, while a significant difference in community structure was observed in ambient seawater inside and outside of the polluted harbor. The microbiome of C. crambe was clearly differentiated from free-living seawater microbes and dominated by Proteobacteria, specifically a single betaproteobacterium that accounted for >86% of all sequence reads. These results indicate that sponge microbiomes exhibit greater stability and pollution tolerance than their free-living microbial counterparts, potentially mitigating the effects of pollutants on coastal marine communities.

Latitudinal variation in the microbiome of the sponge Ircinia campana correlates with host haplotype but not anti-predatory chemical defense

MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections MEPS 565:53-66 (2017) - DOI: https://doi.org/10.3354/meps12015 Latitudinal variation in the microbiome of the sponge Ircinia campana correlates with host haplotype but not anti-predatory chemical defense Clark M. Marino1,2, Joseph R. Pawlik1, Susanna López-Legentil1, Patrick M. Erwin1,* 1Center for Marine Science and Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington, NC 28409, USA 2Present address: Department of Ecology, Evolution, and Marine Biology, University of California Santa Barbara, Santa Barbara, CA 93106, USA *Corresponding author: erwinp@uncw.edu ABSTRACT: Many marine sponges host diverse symbiotic microbial communities that have been implicated in the production of secondary metabolites. These metabolites may defend the host sponge from potential predators. Variability in symbiont communities across the range of the host sponge could alter levels of chemical defense. To investigate the relationship between symbiont composition and chemical defense, the microbiomes and palatability of tissue samples from Ircinia campana were characterized from 5 sites along a latitudinal gradient spanning temperate (South Atlantic Bight, SAB) and tropical (Caribbean) regions. Terminal restriction fragment length polymorphism analysis and Illumina sequencing of 16S ribosomal RNA genes revealed that I. campana from different locations contained significantly distinct microbiomes and exhibited a consistent relationship of lower symbiont similarity over greater geographic distance (i.e. distance-decay). However, crude organic extracts of all samples of I. campana were unpalatable to assay fish Thalassoma bifasciatum in laboratory assays, indicating no difference in chemical defense across locations. Distinct haplotypes of I. campana were detected in populations from the SAB and Caribbean, correlating with the observed patterns of latitudinal variation in microbial symbiont communities. Our findings indicate that I. campana is chemically defended from fish predators across the range of the species and that latitudinal variation occurs in the microbiome of I. campana, driven by a combination of host-specific factors and region-specific environmental filtering of symbiont communities. KEY WORDS: Symbiosis · Microbial community · Chemical defense · Biogeography · Porifera · Intraspecific variation Full text in pdf format Supplement 1 Supplement 2 PreviousNextCite this article as: Marino CM, Pawlik JR, López-Legentil S, Erwin PM (2017) Latitudinal variation in the microbiome of the sponge Ircinia campana correlates with host haplotype but not anti-predatory chemical defense. Mar Ecol Prog Ser 565:53-66. https://doi.org/10.3354/meps12015 Export citation RSS - Facebook - Tweet - linkedIn Cited by Published in MEPS Vol. 565. Online publication date: February 17, 2017 Print ISSN: 0171-8630; Online ISSN: 1616-1599 Copyright © 2017 Inter-Research.

Sponge exhalent seawater contains a unique chemical profile of dissolved organic matter.

Sponges are efficient filter feeders, removing significant portions of particulate and dissolved organic matter (POM, DOM) from the water column. While the assimilation and respiration of POM and DOM by sponges and their abundant microbial symbiont communities have received much attention, there is virtually no information on the impact of sponge holobiont metabolism on the composition of DOM at a molecular-level. We applied untargeted and targeted metabolomics techniques to characterize DOM in seawater samples prior to entering the sponge (inhalant reef water), in samples exiting the sponge (exhalent seawater), and in samples collected just outside the reef area (off reef seawater). Samples were collected from two sponge species, Ircinia campana and Spheciospongia vesparium, on a near-shore hard bottom reef in the Florida Keys. Metabolic profiles generated from untargeted metabolomics analysis indicated that many more compounds were enhanced in the exhalent samples than in the inhalant samples. Targeted metabolomics analysis revealed differences in diversity and concentration of metabolites between exhalent and off reef seawater. For example, most of the nucleosides were enriched in the exhalent seawater, while the aromatic amino acids, caffeine and the nucleoside xanthosine were elevated in the off reef water samples. Although the metabolic profile of the exhalent seawater was unique, the impact of sponge metabolism on the overall reef DOM profile was spatially limited in our study. There were also no significant differences in the metabolic profiles of exhalent water between the two sponge species, potentially indicating that there is a characteristic DOM profile in the exhalent seawater of Caribbean sponges. Additional work is needed to determine whether the impact of sponge DOM is greater in habitats with higher sponge cover and diversity. This work provides the first insight into the molecular-level impact of sponge holobiont metabolism on reef DOM and establishes a foundation for future experimental studies addressing the influence of sponge-derived DOM on chemical and ecological processes in coral reef ecosystems.

Nestedness of hoopoes' bacterial communities: symbionts from the uropygial gland to the eggshell

How microbial symbionts are established and maintain on their hosts is a leading question with important consequences for the understanding of the evolution and functioning of mutualistic relationships. The acquisition by hosts of mutualistic microbial symbionts can be considered as colonization processes of environments (i.e., host) by symbionts. Colonization processes can be explored by characterizing the nestedness of communities, but this approach has rarely been applied to communities of microbial symbionts. We used this approach here, and estimated the nestedness of bacterial communities of hoopoes (Upupa epops), a species with symbiotic bacteria in their uropygial gland that are expected to colonize eggshells where they protect embryos from pathogens. Bacterial communities were characterized by ARISA (Automated rRNA Intergenetic Spacer Region) and studied the nestedness characteristics of bacterial communities living in the uropygial secretion, bill, belly and eggshells of each sampled female hoopoes. We detected a consistent nested pattern of bacterial communities of hoopoes; from the uropygial gland to the eggshell. We also found evidence of study year and reproductive events influencing the level of nestedness of bacterial communities of hoopoes. These results indicate that bacterial communities of eggshells and body parts of female hoopoes are at least partially conditioned by the symbiotic community in the uropygial gland. We discuss the importance of these results for understanding this host–microbial mutualism functioning and evolution.

Intraspecific Variation in Microbial Symbiont Communities of the Sun Sponge, Hymeniacidonheliophila, from Intertidal and Subtidal Habitats

Sponges host diverse and complex communities of microbial symbionts that display a high degree of host specificity. The microbiomes of conspecific sponges are relatively constant, even across distant locations, yet few studies have directly examined the influence of abiotic factors on intraspecific variation in sponge microbial community structure. The contrast between intertidal and subtidal environments is an ideal system to assess the effect of environmental variation on sponge-microbe symbioses, producing two drastically different environments on a small spatial scale. Here, we characterized the microbial communities of individual intertidal and subtidal Hymeniacidon heliophila sponges, ambient seawater, and sediment from a North Carolina oyster reef habitat by partial (Illumina sequencing) and nearly full-length (clone libraries) 16S rRNA gene sequence analyses. Clone library sequences were compared to H. heliophila symbiont communities from the Gulf of Mexico and Brazil, revealing strong host specificity of dominant symbiont taxa across expansive geographic distances. Sediment and seawater samples yielded clearly distinct microbial communities from those found in H. heliophila. Despite the close proximity of the sponges sampled, significant differences between subtidal and intertidal sponges in the diversity, structure, and composition of their microbial communities were detected. Differences were driven by changes in the relative abundance of a few dominant microbial symbiont taxa, as well as the presence or absence of numerous rare microbial taxa. These findings suggest that extreme abiotic fluctuations, such as periodic air exposure in intertidal habitats, can drive intraspecific differences in complex host-microbe symbioses.

Phylogenetic signal in the community structure of host-specific microbiomes of tropical marine sponges.

Sponges (Porifera) can host diverse and abundant communities of microbial symbionts that make crucial contributions to host metabolism. Although these communities are often host-specific and hypothesized to co-evolve with their hosts, correlations between host phylogeny and microbiome community structure are rarely tested. As part of the Earth Microbiome Project (EMP), we surveyed the microbiomes associated with 20 species of tropical marine sponges collected over a narrow geographic range. We tested whether (1) univariate metrics of microbiome diversity displayed significant phylogenetic signal across the host phylogeny; (2) host identity and host phylogeny were significant factors in multivariate analyses of taxonomic and phylogenetic dissimilarity; and (3) different minimum read thresholds impacted these results. We observed significant differences in univariate metrics of diversity among host species for all read thresholds, with strong phylogenetic signal in the inverse Simpson's index of diversity (D). We observed a surprisingly wide range of variability in community dissimilarity within host species (4–73%); this variability was not related to microbial abundance within a host species. Taxonomic and phylogenetic dissimilarity were significantly impacted by host identity and host phylogeny when these factors were considered individually; when tested together, the effect of host phylogeny was reduced, but remained significant. In our dataset, this outcome is largely due to closely related host sponges harboring distinct microbial taxa. Host identity maintained a strong statistical signal at all minimum read thresholds. Although the identity of specific microbial taxa varied substantially among host sponges, closely related hosts tended to harbor microbial communities with similar patterns of relative abundance. We hypothesize that microbiomes with low D might be structured by regulation of the microbial community by the host or by the presence of competitively dominant symbionts that are themselves under selection for host specificity.

Biogeography rather than association with cyanobacteria structures symbiotic microbial communities in the marine sponge Petrosia ficiformis

The sponge Petrosia ficiformis is ubiquitous in the Mediterranean Sea and Eastern Atlantic Ocean, hosting a diverse assemblage of bacteria, including, in illuminated sites, cyanobacteria. Two closely related sponge color morphs have been described, one inside caves and at their entrance (white/pink), and one on the rocky cliffs (violet). The presence of the different morphs and their ubiquity in the Mediterranean (from North-West to South-East) provides an opportunity to examine which factors mostly affect the associated microbial communities in this species: (i) presence of phototrophic symbionts or (ii) biogeography. 16S rRNA gene tag pyrosequencing data of the microbial communities revealed that Chloroflexi, Gammaproteobacteria, and Acidobacteria dominated the bacterial communities of all sponges analyzed. Chlorophyll a content, TEM observations and DNA sequence data confirmed the presence of the cyanobacterium Synechococcus feldmannii in violet and pink morphs of P. ficiformis and their absence in white color morphs. Rather than cyanobacterial symbionts (i.e., color morphs) accounting for variability in microbial symbiont communities, a biogeographic trend was observed between P. ficiformis collected in Israel and Italy. Analyses of partial 18S rRNA and mitochondrial cytochrome c oxidase subunit I (COX1) gene sequences revealed consistent genetic divergence between the violet and pink-white morphotypes of P. ficiformis. Overall, data indicated that microbial symbiont communities were more similar in genetically distinct P. ficiformis from the same location, than genetically similar P. ficiformis from distant locations.

Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts.

Microorganisms often form symbiotic relationships with eukaryotes, and the complexity of these relationships can range from those with one single dominant symbiont to associations with hundreds of symbiont species. Microbial symbionts occupying equivalent niches in different eukaryotic hosts may share functional aspects, and convergent genome evolution has been reported for simple symbiont systems in insects. However, for complex symbiont communities, it is largely unknown how prevalent functional equivalence is and whether equivalent functions are conducted by evolutionarily convergent mechanisms. Sponges represent an evolutionarily divergent group of species with common physiological and ecological traits. They also host complex communities of microbial symbionts and thus are the ideal model to test whether functional equivalence and evolutionary convergence exist in complex symbiont communities across phylogenetically divergent hosts. Here we use a sampling design to determine the phylogenetic and functional profiles of microbial communities associated with six sponge species. We identify common functions in the six microbiomes, demonstrating the existence of functional equivalence. These core functions are consistent with our current understanding of the biological and ecological roles of sponge-associated microorganisms and also provide insight into symbiont functions. Importantly, core functions also are provided in each sponge species by analogous enzymes and biosynthetic pathways. Moreover, the abundance of elements involved in horizontal gene transfer suggests their key roles in the genomic evolution of symbionts. Our data thus demonstrate evolutionary convergence in complex symbiont communities and reveal the details and mechanisms that underpin the process.