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

Gloeckner, Volker; Wehrl, Markus; Moitinho‐Silva, Lucas; Gernert, Christine; Schupp, Peter J.; Pawlik, Joseph R.; Lindquist, Niels; Erpenbeck, Dirk; Wörheide, Gert; Hentschel, Ute

doi:10.1086/bblv227n1p78

Cited by 196 publications

(240 citation statements)

References 46 publications

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“…Previous studies have categorized H. heliophila as a low-microbial-abundance (LMA) sponge on the basis of transmission electronmicroscopic observations and microbial species composition (29,31). The latter is consistent with our results, as bacterial communities associated with LMA sponges tend to be dominated by Proteobacteria or Cyanobacteria (47,48). In addition, the phyla Planctomycetes, Cyanobacteria, and Deferribacteres were common members of the H. heliophila microbiome.…”

Section: Discussionsupporting

confidence: 90%

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

Weigel

Erwin

2016

Appl Environ Microbiol

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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. Sponges form ancient symbioses (as described in reference 1) with a great diversity of bacterial, archaeal, and eukaryotic microorganisms (1, 2). Most of these microbial symbionts elude cultivation (3); thus, culture-independent techniques such as next-generation DNA sequencing are necessary to elucidate the immense diversity of microbial communities in marine sponges. For example, the sponge Rhopaloeides odorabile hosts nearly 3,000 unique microbial taxa (4). Symbiotic microbes can constitute up to 40% of the sponge mesohyl volume (5) and perform a variety of ecological functions in the host sponge (6). Sponge-associated microbial symbionts may play roles in the nutrient acquisition, chemical defense production, antifouling activity, and disease susceptibility of host sponges (1, 7). Despite the ubiquity of microbial symbionts in sponges, much is still unknown about their structure and ecological function.Sponges host microbial communities that are distinct from those found in seawater and exhibit a high degree of host specificity (4, 8, 9), even between closely related sponge species (10). Determining what structures these symbiotic communities is a current research priority, because it will provide insight into the maintenance of one of the most ancient metazoan-microbial symbio...

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Section: Discussionsupporting

confidence: 90%

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

Weigel

Erwin

2016

Appl Environ Microbiol

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“…Therefore, sponge tissue with this level of d 15 N would suggest N 2 fixation by the microbial symbionts (22,46). Accordingly, the high d 15 N values found for LMA sponges from the Florida Keys (46) suggest no or negligible N 2 fixation in these sponges, a finding which falls in line with our findings of high d 15 N levels and no measurable N 2 fixation in the Mediterranean LMA sponges. Of the sponges examined, only the HMA species C. reniformis showed a low d 15 N of 2‰, potentially indicating nitrogen import through N 2 fixation.…”

Section: Discussionsupporting

confidence: 85%

“…Sponges have been categorized as those with a high microbial abundance (HMA) and those with a low microbial abundance (LMA) (12), where HMA species harbor dense, diverse microbial communities and LMA species contain fewer and less diverse microorganisms (6,(13)(14)(15). Despite their distinct microbial compositions, HMA and LMA sponges show similar functional gene repertoires, which has been interpreted to be a functional convergence between the two microbiome types (10,11,16).…”

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confidence: 99%

Microbial Diversity and Putative Diazotrophy in High- and Low-Microbial-Abundance Mediterranean Sponges

Ribes

Dziallas

Coma

et al. 2015

Appl Environ Microbiol

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c Microbial communities associated with marine sponges carry out nutrient transformations essential for benthic-pelagic coupling; however, knowledge about their composition and function is still sparse. We evaluated the richness and diversity of prokaryotic assemblages associated with three high-microbial-abundance (HMA) and three low-microbial-abundance (LMA) sympatric Mediterranean sponges to address their stability and uniqueness. Moreover, to examine functionality and because an imbalance between nitrogen ingestion and excretion has been observed for some of these species, we sequenced nitrogenase genes (nifH) and measured N 2 fixation. The prokaryotic communities in the two sponge types did not differ in terms of richness, but the highest diversity was found in HMA sponges. Moreover, the discrete composition of the communities in the two sponge types relative to that in the surrounding seawater indicated that horizontal transmission and vertical transmission affect the microbiomes associated with the two sponge categories. nifH genes were found in all LMA species and sporadically in one HMA species, and about half of the nifH gene sequences were common between the different sponge species and were also found in the surrounding water, suggesting horizontal transmission.15 N 2 -enriched incubations showed that N 2 fixation was measurable in the water but was not associated with the sponges. Also, the analysis of the isotopic ratio of 15 N to 14 N in sponge tissue indicated that N 2 fixation is not an important source of nitrogen in these Mediterranean sponges. Overall, our results suggest that compositional and functional features differ between the prokaryotic communities associated with HMA and LMA sponges, which may affect sponge ecology. Marine sponges are sessile filter-feeder metazoans that dominate many hard-bottom benthic substrates around the world (1, 2). They filter large volumes of water and efficiently clear particles down to less than 2 m in size (see reference 3 and references therein). Sponges host complex microbial communities that are generally specific, stable, and distinct in composition compared with the characteristics of the microbes in the surrounding seawater (4-7). Their acquisition can be through horizontal transmission from the surrounding water or by vertical transmission, where microbes are transferred from parental sponges to progeny (6,8).Sponge-associated microbes can supply limiting nutrients to the host and process metabolic waste from the host (4, 9, 10), but the rich taxonomy and functional genetic potential of the sponge-associated microbes suggest that they carry out additional functions (11). Sponges have been categorized as those with a high microbial abundance (HMA) and those with a low microbial abundance (LMA) (12), where HMA species harbor dense, diverse microbial communities and LMA species contain fewer and less diverse microorganisms (6,(13)(14)(15). Despite their distinct microbial compositions, HMA and LMA sponges show similar functional gene repertoires, whic...

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“…The proteobacterial OTUs are dominated in adult A. queenslandica by classes Beta-and Gamma-proteobacteria, as observed in several species of low microbial abundance (LMA) sponge (Hentschel et al, 2003;Giles et al, 2012), rather than the more generally observed dominance by Gamma-and Alpha-classes (Thomas et al, 2016). Together, these observations indicate that A. queenslandica is appropriately considered as a LMA sponge species, as has been reported for congeners (Gloeckner et al, 2014;Poppell et al, 2014).…”

Section: Amphimedon Queenslandica Adults House a Low Complexity Microsupporting

confidence: 54%

Ontogenetic Changes in the Bacterial Symbiont Community of the Tropical Demosponge Amphimedon queenslandica: Metamorphosis Is a New Beginning

et al. 2016

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Vertical transmission of bacterial symbionts, which is known in many species of sponge (Porifera), is expected to promote strong fidelity between the partners. Combining 16S rRNA gene amplicon sequencing and electron microscopy, we have assayed the relative abundance of vertically-inherited bacterial symbionts in several stages of the life cycle of Amphimedon queenslandica, a tropical coral reef sponge. We reveal that adult A. queenslandica house a low diversity microbiome dominated by just three proteobacterial OTUs, with a single gammaprotebacterium clearly dominant through much of the life cycle. This ontogenetic perspective has revealed that, although vertical transmission occurs very early in development, the inherited symbionts do not maintain proportional dominance of the bacterial community at every developmental stage. A reproductive bottleneck in the A. queenslandica life cycle is larval settlement, when a free-swimming pelagic larva settles out of the water column onto the benthos and completes metamorphoses into the sessile body plan within just 3-4 days. During this dramatic life cycle transition, an influx of environmentally-derived bacteria leads to a major reorganization of the microbiome, potentially challenging the fidelity and persistence of the vertically-inherited symbiotic relationships. However, dominance of the primary, vertically-inherited symbionts is restored in adult sponges. The mechanisms underlying ontogenetic changes in the bacterial community are unknown, including how the dominance of the primary symbionts is restored in the adult sponge-does the host or symbiont regulate this process? Using high-resolution transcriptional profiling in multiple stages of the A. queenslandica life cycle combined with this natural perturbation of the microbiome immediately following larval settlement, we are beginning to identify candidate host genes associated with animal-bacterial crosstalk. Among the sponge host genes upregulated during the times of active microbiome assembly, there is an enrichment of genes potentially involved in innate immunity, including scavenger receptors, and of genes containing eukaryote-like domains, which have elsewhere Fieth et al.Sponge Microbiome Changes through Lifecycle been implicated in host-symbiont interactions. Intriguingly, we also see an enrichment of sponge genes arising from ancient horizontal transfer events from bacteria, which raises the possibility that host-bacterial associations in the evolutionary past may help to regulate host-bacterial associations in the ecological present.

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

Cited by 196 publications

References 46 publications

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

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

Microbial Diversity and Putative Diazotrophy in High- and Low-Microbial-Abundance Mediterranean Sponges

Ontogenetic Changes in the Bacterial Symbiont Community of the Tropical Demosponge Amphimedon queenslandica: Metamorphosis Is a New Beginning

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