Low Microbial Abundance Sponges Research Articles

Size Effects on Pumping Rates in High Microbial versus Low Microbial Abundance Marine Sponges

Sponges are increasingly recognized as ecologically important on coral reefs as scleractinian corals decline. Most sponge species can be divided into two symbiotic phenotypes which are characterized as high microbial abundance (HMA) or low microbial abundance (LMA) sponges. Sponge species of HMA or LMA symbiotic phenotypes differ not just in their microbiomes, but in other characteristics, including that LMA sponges actively pump at higher rates than HMA sponges based on a standard normalization to size. This dichotomy has recently been questioned because the size range of LMA sponges used to quantify pumping rates during studies on their trophic ecology were exceedingly small, often less than an order of magnitude. Here, both HMA and LMA sponges, across two to three orders of magnitude in sponge volume (mL) or mass (g) were assessed for allometric relationships between sponge size and pumping rates (Q = mL s−1). The scaling analysis of all data sets combined reveals that HMA sponges scale their pumping rates isometrically with size, while LMA sponges scale their pumping rate allometrically. When HMA species are examined separately, however, tropical HMA sponges scaled isometrically, while temperate HMA sponges scaled allometrically. From an ecological perspective, to quantify differences between HMA and LMA sponges for rate functions of interest (e.g., feeding) it is important to remove the effects of size as a covariate, and adjust the Q values of sponges to a standard volume or mass. For multiple species and geographic locations, this analysis shows that LMA sponges always maintain higher Q values. On tropical coral reefs, the differences between HMA and LMA sponges are intrinsic and constrained by strong evolutionary selection resulting in fixed differences in Q, regardless of sponge size.

The removal of dissolved organic matter by marine sponges is a function of its composition and concentration: An in situ seasonal study of four Mediterranean species

Sponges are unique among metazoans in their ability to use dissolved organic matter (DOM), the largest pool of organic matter in the ocean, as a major food source. The effect of variations in DOM abundance and composition on its uptake by sponges has rarely been studied. We examined, in situ, the seasonal uptake of DOM by four sponges [2 species with high microbial abundance (HMA) and 2 with low microbial abundance (LMA)] in the northwestern Mediterranean. Dissolved organic carbon (DOC) showed a strong seasonality with 3-fold higher concentrations in fall-winter (256 ± 16 μmol L−1, mean ± SE) than in spring-summer (88 ± 3 μmol L−1). Dissolved organic nitrogen (DON) showed the opposite trend, with higher summer concentrations (8.9 ± 0.4 μmol L−1) and mean concentrations of 2.5–3.4 μmol L−1 in the other seasons. DOC removal by all sponge species increased linearly with its ambient concentration, but only above a DOC removal threshold that was threefold higher in fall-winter (198 μmol L−1) than in spring-summer (74 μmol L−1). All species showed a concentration-dependent DON removal, but LMA sponges removed more DON than HMA sponges. The DOC removal rate (normalized to sponge volume) was 2–3 times higher in fall-winter, when ambient DOC levels were high, than in spring-summer. Sponges efficiently removed clusters of the fluorescent DOM (FDOM) associated with protein-rich DOM, but not those associated with humic material. The clear threshold for DOC removal and the protein-like FDOM uptake pattern suggest that the quality and quantity of DOM control its removal and transformation by marine sponges. Our results indicate that marine sponges transform the composition of the coastal DOM pool, thereby affecting its fate. It is postulated that the DOM excreted by the sponges is more recalcitrant; consequently, sponge activity enhances carbon sequestration in benthic habitats in a similar fashion to that of the oceanic ‘microbial pump’.

Microbiome diversity and metabolic capacity determines the trophic ecology of the holobiont in Caribbean sponges

Sponges are increasingly recognized as an ecologically important taxon on coral reefs, representing significant biomass and biodiversity where sponges have replaced scleractinian corals. Most sponge species can be divided into two symbiotic states based on symbiont community structure and abundance (i.e., the microbiome), and are characterized as high microbial abundance (HMA) or low microbial abundance (LMA) sponges. Across the Caribbean, sponge species of the HMA or LMA symbiotic states differ in metabolic capacity, as well as their trophic ecology. A metagenetic analysis of symbiont 16 S rRNA and metagenomes showed that HMA sponge microbiomes are more functionally diverse than LMA microbiomes, offer greater metabolic functional capacity and redundancy, and encode for the biosynthesis of secondary metabolites. Stable isotope analyses showed that HMA and LMA sponges primarily consume dissolved organic matter (DOM) derived from external autotrophic sources, or live particulate organic matter (POM) in the form of bacterioplankton, respectively, resulting in a low degree of resource competition between these symbiont states. As many coral reefs have undergone phase shifts from coral- to macroalgal-dominated reefs, the role of DOM, and the potential for future declines in POM due to decreased picoplankton productivity, may result in an increased abundance of chemically defended HMA sponges on tropical coral reefs.

Fluxes of the Amazon River plume nutrients and microbes into marine sponges

Sponges have co-evolved with microbes for over 400 myr. Previous studies have demonstrated that sponges can be classified according to the abundance of microbes in their tissues as Low Microbial Abundance (LMA) and High Microbial Abundance (HMA). While LMA sponges rely mainly on water column microbes, HMA appear to rely much more on symbiotic fermentative and autotrophic microbes maintained in their tissues. However, it is unclear if this pattern holds when comparing different species of tropical sponges under extreme nutrient conditions and sediment loads in the water column, such as the Great Amazon Reef System (GARS), which covers an area of ~56,000 km2 off the Amazon River mouth. Sponges are the major GARS benthic components. However, these sponges' microbiome across the GARS is still unknown. Here, we investigated water quality, isotopic values (δ13C and δ15N), metagenomic and lipidomic profiles of sponges obtained from different sectors throughout the GARS. >180 million shotgun metagenomic reads were annotated, covering 22 sponge species. Isotopic and lipidomic analyses suggested LMA sponges rely on the Amazon River Plume for nutrition. HMA sponges (N = 15) had higher Roseiflexus and Nitrospira abundance, whereas LMA sponges (N = 7) had higher Prochlorococcus and Pelagibacter abundance. Functional data revealed that the LMA sponge microbiomes had greater number of sequences related to phages and prophages as well as electron transport and photophosphorylation which may be related to photosynthetic processes associated with the Prochlorococcus and Synechococcus found in the LMA. The higher phages abundance in LMA sponges could be related to these holobionts' reduced defense towards phage infection. Meanwhile, HMA sponge microbiomes had higher Clustered Regularly Interspaced Short Palindromic Repeats-CRISPR abundance, which may be involved in defense against phage infection. This study sheds light on the nutrient fluxes and microbes from the Amazon River plume into the sponge holobionts.

The important role of sponges in carbon and nitrogen cycling in a deep‐sea biological hotspot

Abstract Deep‐sea sponge grounds are hotspots of biodiversity, harbouring thriving ecosystems in the otherwise barren deep sea. It remains unknown how these sponge grounds survive in this food‐limited environment. Here, we unravel how sponges and their associated fauna sustain themselves by identifying their food sources and food‐web interactions using bulk and compound‐specific stable isotope analysis of amino and fatty acids. We found that sponges with a high microbial abundance had an isotopic composition resembling organisms at the base of the food web, suggesting that they are able to use dissolved resources that are generally inaccessible to animals. In contrast, low microbial abundance sponges had a bulk isotopic composition that resembles a predator at the top of a food web, which appears to be the result of very efficient recycling pathways that are so far unknown. The compound‐specific‐isotope analysis, however, positioned low‐microbial abundance sponges with other filter‐feeding fauna. Furthermore, fatty‐acid analysis confirmed transfer of sponge‐derived organic material to the otherwise food‐limited associated fauna. Through this subsidy, sponges are key to the sustenance of thriving deep‐sea ecosystems and might have, due to their ubiquitous abundance, a global impact on biogeochemical cycles. Read the free Plain Language Summary for this article on the Journal blog.

Bacterial composition and putative functions associated with sponges, sediment and seawater from the Tioman coral reef system, Peninsular Malaysia

ABSTRACT Microbial communities associated with sponges play important roles in sponge health, defence and nutrient dynamics in coral reef systems. Here, we used a 16S rRNA gene high-throughput sequencing approach in order to test for differences in bacterial composition and predictive functional differences among two LMA (low microbial abundance) (Stylissa carteri and Stylissa massa), one well-known HMA (high microbial abundance) (Xestospongia testudinaria), one putative HMA (Aaptos lobata) sponge species, sediment and seawater in a coral reef ecosystem surrounding Tioman Island. Our results showed that biotope (sponge species, sediment and seawater) was a significant predictor of composition and abundance of bacterial communities. Proteobacteria was the dominant phylum in S. carteri, seawater, sediment and A. lobata, whilst bacterial communities of S. massa and X. testudinaria were dominated by Cyanobacteria and Chloroflexi, respectively. The predicted metagenome revealed differentially enriched pathways in HMA and LMA sponges. Differentially enriched subcategories in HMA sponges included ‘Signaling Molecules and Interaction’, ‘Carbohydrate Metabolism’ and ‘Excretory System’. Subcategories enriched in LMA sponges included ‘Replication and Repair’, ‘Energy Metabolism’, ‘Metabolism of Cofactors and Vitamins’ and ‘Environmental Adaptation’. Overall, the predicted functional analysis suggests that, although HMA and LMA associated bacterial communities shared core functional features, they use different strategies to defend against pathogens, obtain energy or cope with stress.

Differential processing of dissolved and particulate organic matter by deep-sea sponges and their microbial symbionts

Deep-sea sponges create hotspots of biodiversity and biological activity in the otherwise barren deep-sea. However, it remains elusive how sponge hosts and their microbial symbionts acquire and process food in these food-limited environments. Therefore, we traced the processing (i.e. assimilation and respiration) of 13C- and 15N-enriched dissolved organic matter (DOM) and bacteria by three dominant North Atlantic deep-sea sponges: the high microbial abundance (HMA) demosponge Geodia barretti, the low microbial abundance (LMA) demosponge Hymedesmia paupertas, and the LMA hexactinellid Vazella pourtalesii. We also assessed the assimilation of both food sources into sponge- and bacteria-specific phospholipid-derived fatty acid (PLFA) biomarkers. All sponges were capable of assimilating DOM as well as bacteria. However, processing of the two food sources differed considerably between the tested species: the DOM assimilation-to-respiration efficiency was highest for the HMA sponge, yet uptake rates were 4–5 times lower compared to LMA sponges. In contrast, bacteria were assimilated most efficiently and at the highest rate by the hexactinellid compared to the demosponges. Our results indicate that phylogeny and functional traits (e.g., abundance of microbial symbionts, morphology) influence food preferences and diet composition of sponges, which further helps to understand their role as key ecosystem engineers of deep-sea habitats.

Viral ecogenomics across the Porifera

BackgroundViruses directly affect the most important biological processes in the ocean via their regulation of prokaryotic and eukaryotic populations. Marine sponges form stable symbiotic partnerships with a wide diversity of microorganisms and this high symbiont complexity makes them an ideal model for studying viral ecology. Here, we used morphological and molecular approaches to illuminate the diversity and function of viruses inhabiting nine sponge species from the Great Barrier Reef and seven from the Red Sea.ResultsViromic sequencing revealed host-specific and site-specific patterns in the viral assemblages, with all sponge species dominated by the bacteriophage order Caudovirales but also containing variable representation from the nucleocytoplasmic large DNA virus families Mimiviridae, Marseilleviridae, Phycodnaviridae, Ascoviridae, Iridoviridae, Asfarviridae and Poxviridae. Whilst core viral functions related to replication, infection and structure were largely consistent across the sponge viromes, functional profiles varied significantly between species and sites largely due to differential representation of putative auxiliary metabolic genes (AMGs) and accessory genes, including those associated with herbicide resistance, heavy metal resistance and nylon degradation. Furthermore, putative AMGs varied with the composition and abundance of the sponge-associated microbiome. For instance, genes associated with antimicrobial activity were enriched in low microbial abundance sponges, genes associated with nitrogen metabolism were enriched in high microbial abundance sponges and genes related to cellulose biosynthesis were enriched in species that host photosynthetic symbionts.ConclusionsOur results highlight the diverse functional roles that viruses can play in marine sponges and are consistent with our current understanding of sponge ecology. Differential representation of putative viral AMGs and accessory genes across sponge species illustrate the diverse suite of beneficial roles viruses can play in the functional ecology of these complex reef holobionts.3fNQJtcyRuwttbnAh9LNMAVideo

Trophic niche separation that facilitates co‐existence of high and low microbial abundance sponges is revealed by in situ study of carbon and nitrogen fluxes

Trophic niche separation that facilitates co‐existence of high and low microbial abundance sponges is revealed by in situ study of carbon and nitrogen fluxes

In situ determination of Si, N, and P utilization by the demosponge Tethya citrina: A benthic-chamber approach

Sponges consume dissolved silicon (DSi) to build their skeletons. Few studies have attempted to quantify DSi utilization by these organisms and all available determinations come from laboratory measurements. Here we measured DSi consumption rates of the sponge Tethya citrina in its natural habitat, conducting 24h incubations in benthic chambers. Sponges consumed DSi at an average rate of 0.046 ± 0.018 μmol h-1 mL-1 when DSi availability in its habitat was 8.3 ± 1.8 μM. Such DSi consumption rates significantly matched the values predicted by a kinetic model elsewhere developed previously for this species through laboratory incubations. These results support the use of laboratory incubations as a suitable approach to learn about DSi consumption. During the field incubations, utilization of other dissolved inorganic nutrients by this low-microbial-abundance (LMA) sponge was also measured. The sponges were net sources of ammonium (-0.043 ± 0.031 μmol h-1 mL-1), nitrate (-0.063 ± 0.031 μmol h-1 mL-1), nitrite (-0.007 ± 0.003 μmol h-1 mL-1), and phosphate (-0.004 ± 0.005 μmol h-1 mL-1), in agreement with the general pattern in other LMA species. The detected effluxes were among the lowest reported for sponges, which agreed with the low respiration rates characterizing this species (0.35 ± 0.11 μmol-O2 h-1 mL-1). Despite relatively low flux, the dense population of T. citrina modifies the availability of dissolved inorganic nutrients in the demersal water of its habitat, contributing up to 14% of nitrate and nitrite stocks. Through these effects, the bottom layer contacting the benthic communities where siliceous LMA sponges abound can be partially depleted in DSi, but can benefit from inputs of N and P dissolved inorganic nutrients that are critical to primary producers.

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.

Dissolved inorganic nitrogen fluxes from common Florida Bay (U.S.A.) sponges

AbstractSponge biomass represents the largest heterotrophic component of benthic biota in the Florida Bay ecosystem. These organisms can significantly alter the water quality of their surrounding environment through biogeochemical transformations of nutrient elements resulting from their dynamic pumping, water filtration, and respiration processes. Ammonium (NH4+) and nitrate plus nitrite (NO3− + NO2−; NO x−) fluxes were obtained for 11 ecologically important species at three sites within Florida Bay, Florida (U.S.A.) utilizing chamber incubations on undisturbed individual sponges. Significant dissolved inorganic nitrogen (DIN) effluxes ranging between 9.0 ± 2.2 μmol N h−1 Lsponge−1 and 141 ± 26 μmol N h−1 Lsponge−1 were observed for eight of the 11 tested sponges; specifically, from six of eight tested high‐microbial abundance (HMA) sponges, and from two of three tested low‐microbial abundance (LMA) sponges. The abundant HMA species Chondrilla nucula showed the highest, volume‐normalized rate of DIN release. These fluxes represent a continuation of the previously observed dichotomy in the chemical speciation of DIN in exhalent waters of LMA and HMA sponges, with NH4+ and NO x− dominating their respective exhalent jets. Surprisingly, we found that dissolved organic matter (DOM) appeared to make a negligible contribution to the total released N, but we hypothesize that the lack of DOM utilization or production was due to methodological limitations. Our flux data combined with sponge biomass estimates indicate that sponges, particularly HMA species, are a large, and potentially dominant, source of inorganic nitrogen to Florida Bay waters.

Compositional analysis of archaeal communities in high and low microbial abundance sponges in the Misool coral reef system, Indonesia

ABSTRACTThe high/low microbial abundance (HMA/LMA) dichotomy in sponges has been the subject of several studies over recent years, but few studies have analysed this dichotomy in terms of the sponge archaeal community and function. Using a 16S rRNA gene barcoded pyrosequencing approach and predictive functional analysis (PICRUSt) we compared the archaeal composition, richness and predicted function of one HMA sponge (Xestospongia testudinaria), one LMA sponge (Stylissa carteri) and one sponge species of unknown microbial abundance (Aaptos lobata). Although most of the archaeal sequences were assigned to the Crenarchaeota phylum, S. carteri had the highest percentage of sequences assigned to the Euryarchaeota phylum. Variation among sponge species explained >85% of the variation in archaeal operational taxonomic unit (OTU) composition with each sponge species forming a distinct cluster. There were significant differences in predicted PICRUSt profiles among sponge species, suggesting that archaeal communities present in the studied sponge species may perform different functions. X. testudinaria and A. lobata were similar both in terms of OTU and KEGG orthologues composition, which may indicate that A. lobata is a HMA sponge. Additionally, some of the most enriched functions seem to be related to traits associated with high and low microbial abundance sponges.

Trophic niche separation that facilitates co‐existence of high and low microbial abundance sponges is revealed by in situ study of carbon and nitrogen fluxes

AbstractSponges are commonly divided into high (HMA) and low (LMA) microbial‐abundance species according to the bacterial biomass in their tissue. These two groups reflect distinct aquiferous structures and feeding strategies. In the NW Mediterranean coralligenous community, HMA and LMA sponges are often packed in dense, multispecies assemblages that cover many pinnacles and overhangs. We investigated the metabolism of HMA and LMA species that cohabitate the coralligenous community by sampling in situ the inhaled and exhaled water. Sponges consumed plankton, dissolved organic carbon (DOC), and ammonium in relation to their abundance in ambient water. The plankton retention efficiency was high for all species. DOC was the main source of C for the sponge species, accounting for ∼ 90% of the examined sources. Nitrogen fluxes markedly differed between the two groups: plankton was the main source of nitrogen for LMAs that excreted dissolved organic nitrogen (DON) and ammonium. The nitrogenous waste products of LMAs were found to be the major source of nitrogen (up to 97%) for HMAs that efficiently removed DON and ammonium and excreted nitrate. The different capacity of both sponge strategies to use dissolved resources suggests a partial trophic niche separation related to HMA‐LMA dichotomy as a mechanism facilitating their dense co‐existence in the community. Our findings suggest that a mixed assemblage of sponges (and their associated microbes) is able to utilize the suspended particulate and dissolved material more efficiently than a single species population and may contribute to the understanding of the phenomena of the stability and diversity of dense sponge assemblages in oligotrophic habitats.

Predicting the HMA-LMA Status in Marine Sponges by Machine Learning.

The dichotomy between high microbial abundance (HMA) and low microbial abundance (LMA) sponges has been observed in sponge-microbe symbiosis, although the extent of this pattern remains poorly unknown. We characterized the differences between the microbiomes of HMA (n = 19) and LMA (n = 17) sponges (575 specimens) present in the Sponge Microbiome Project. HMA sponges were associated with richer and more diverse microbiomes than LMA sponges, as indicated by the comparison of alpha diversity metrics. Microbial community structures differed between HMA and LMA sponges considering Operational Taxonomic Units (OTU) abundances and across microbial taxonomic levels, from phylum to species. The largest proportion of microbiome variation was explained by the host identity. Several phyla, classes, and OTUs were found differentially abundant in either group, which were considered “HMA indicators” and “LMA indicators.” Machine learning algorithms (classifiers) were trained to predict the HMA-LMA status of sponges. Among nine different classifiers, higher performances were achieved by Random Forest trained with phylum and class abundances. Random Forest with optimized parameters predicted the HMA-LMA status of additional 135 sponge species (1,232 specimens) without a priori knowledge. These sponges were grouped in four clusters, from which the largest two were composed of species consistently predicted as HMA (n = 44) and LMA (n = 74). In summary, our analyses shown distinct features of the microbial communities associated with HMA and LMA sponges. The prediction of the HMA-LMA status based on the microbiome profiles of sponges demonstrates the application of machine learning to explore patterns of host-associated microbial communities.

Compositional analysis of bacterial communities in seawater, sediment, and sponges in the Misool coral reef system, Indonesia

Sponge species have been deemed high microbial abundance (HMA) or low microbial abundance (LMA) based on the composition and abundance of their microbial symbionts. In the present study, we evaluated the richness and composition of bacterial communities associated with one HMA sponge (Xestospongia testudinaria; Demospongiae: Haplosclerida: Petrosiidae), one LMA sponge (Stylissa carteri; Demospongiae: Scopalinida - Scopalinidae), and one sponge with a hitherto unknown microbial community (Aaptos suberitoides; Demospongiae: Suberitida: Suberitidae) inhabiting the Misool coral reef system in the West Papua province of Indonesia. The bacterial communities of these sponge species were also compared with seawater and sediment bacterial communities from the same coastal coral reef habitat. Using a 16S rRNA gene barcoded pyrosequencing approach, we showed that the most abundant phylum overall was Proteobacteria. The biotope (sponge species, sediment or seawater) explained almost 84% of the variation in bacterial composition with highly significant differences in composition among biotopes and a clear separation between bacterial communities from seawater and S. carteri; X. testudinaria and A. suberitoides and sediment. The Chloroflexi classes SAR202 and Anaerolineae were most abundant in A. suberitoides and X. testudinaria and both of these species shared several OTUs that were largely absent in the remaining biotopes. This suggests that A. suberitoides is a HMA sponge. Although similar, the bacterial communities of S. carteri and seawater were compositionally distinct. These results confirm compositional differences between sponge and non-sponge biotopes and between HMA and LMA sponges.

Trophic ecology of sponges from shallow to mesophotic depths (3 to 150 m): Comment on Pawlik et al. (2015)

Pawlik et al. (2015; Mar Ecol Prog Ser 519:265�283) proposed 4 hypotheses regarding the influence of food limitation on growth and distribution of Caribbean sponges: (1) increasing sponge cover as particulate organic carbon increases with depth, (2) replacement of high microbial abundance sponges with low microbial abundance sponges at depth, (3) dominance of sponges with photosymbionts above the photosynthetic compensation point, and (4) sponge morphologies that reflect adaptations to feeding. Pawlik et al. (2015) concluded that there is no evidence of food limitation (i.e. bottom-up control), and that predation is the primary process that determines the growth, biomass and biodiversity of sponges on Caribbean coral reefs. Here, we address the con- clusions of Pawlik et al. (2015) in the context of the observational, correlational, and manipulative studies they utilized in their analysis. We argue that both top-down (predation pressure) and bot- tom-up (food limitation) processes influence the distribution of sponges on coral reefs, that these factors vary in time and space, and that only when multifactorial manipulative experiments are undertaken will the magnitude of the roles of predation and food limitation be understood.

GeoChip-based insights into the microbial functional gene repertoire of marine sponges (high microbial abundance, low microbial abundance) and seawater.

The GeoChip 4.2 gene array was employed to interrogate the microbial functional gene repertoire of sponges and seawater collected from the Red Sea and the Mediterranean. Complementary amplicon sequencing confirmed the microbial community composition characteristic of high microbial abundance (HMA) and low microbial abundance (LMA) sponges. By use of GeoChip, altogether 20,273 probes encoding for 627 functional genes and representing 16 gene categories were identified. Minimum curvilinear embedding analyses revealed a clear separation between the samples. The HMA/LMA dichotomy was stronger than any possible geographic pattern, which is shown here for the first time on the level of functional genes. However, upon inspection of individual genes, very few specific differences were discernible. Differences were related to microbial ammonia oxidation, ammonification, and archaeal autotrophic carbon fixation (higher gene abundance in sponges over seawater) as well as denitrification and radiation-stress-related genes (lower gene abundance in sponges over seawater). Except for few documented specific differences the functional gene repertoire between the different sources appeared largely similar. This study expands previous reports in that functional gene convergence is not only reported between HMA and LMA sponges but also between sponges and seawater.

About the Cover.

Next article FreeAbout the CoverPDFPDF PLUSFull Text Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinked InRedditEmailQR Code SectionsMoreCoverSponges (Porifera) represent an evolutionarily ancient phylum with a fossil record dating back to Precambrian times. Many sponges harbor dense and diverse microbial consortia extracellularly within their tissues. In contrast to these “high microbial abundance sponges” (HMA), the tissues of the so-called “low microbial abundance sponges” (LMA) are nearly devoid of microorganisms. The sponge on the cover, Ircinia sp., from the Mediterranean Sea, belongs to the HMA category. This scanning electron microscopy image shows the main skeleton structures, which are surrounded by thin, fibrillar, collagenous spongin, making up the bulk of the sponge tissue. Microorganisms are not visible at this magnification.HMA and LMA sponges may occur on the same reef in close proximity. Recent studies have shown that HMA sponges differ from their LMA counterparts in more than just the number and diversity of microorganisms they contain. For example, the HMA sponges appear to be less well irrigated. While the HMA sponge tissue displays fewer canals and smaller choanocyte chambers, the extracellular matrix is greatly expanded. The HMA/LMA dichotomy has long been recognized; however, the reasons for this pattern remain unknown.In this issue, Hentschel and collaborators examined sponge species from three locations for the presence of microorganisms in the sponge mesohyl matrix (pages 78–88). Of more than 50 sponge species investigated, half belonged to the HMA and half to the LMA category. The HMA/LMA dichotomy was also investigated in the taxonomic framework of their animal hosts, but a clear phylogenetic pattern could not be identified. This survey significantly expands previous datasets, serves as a reference database for anyone interested in bacterial abundances in sponges, and contributes to a better understanding of sponge-microbe symbioses.Credits: Cover photo ©S. Diller, Scientific Photography, Wuerzburg, 2014 (see http://www.vimeo.com/100428013 for “nanoflight” videos of sponges); cover design, Beth Liles, Marine Biological Laboratory. Next article DetailsFiguresReferencesCited by The Biological Bulletin Volume 227, Number 1August 2014 Published in association with the Marine Biological Laboratory Article DOIhttps://doi.org/10.1086/BBLv227n1cover © 2014 by Marine Biological Laboratory. All rights reserved.PDF download Crossref reports no articles citing this article.

The HMA-LMA Dichotomy Revisited: an Electron Microscopical Survey of 56 Sponge Species

The dichotomy between high microbial abundance (HMA) and low microbial abundance (LMA) sponges has been long recognized. In the present study, 56 sponge species from three geographic regions (greater Caribbean, Mediterranean, Red Sea) were investigated by transmission electron microscopy for the presence of microorganisms in the mesohyl matrix. Additionally, bacterial enumeration by DAPI-counting was performed on a subset of samples. Of the 56 species investigated, 28 were identified as belonging to the HMA and 28 to the LMA category. The sponge orders Agelasida and Verongida consisted exclusively of HMA species, and the Poecilosclerida were composed only of LMA sponges. Other taxa contained both types of microbial associations (e.g., marine Haplosclerida, Homoscleromorpha, Dictyoceratida), and a clear phylogenetic pattern could not be identified. For a few sponge species, an intermediate microbial load was determined, and the microscopy data did not suffice to reliably determine HMA or LMA status. To experimentally determine the HMA or LMA status of a sponge species, we therefore recommend a combination of transmission electron microscopy and 16S rRNA gene sequence data. This study significantly expands previous reports on microbial abundances in sponge tissues and contributes to a better understanding of the HMA-LMA dichotomy in sponge-microbe symbioses.