In general, there was a positive linear relationship between richness and evenness, among biotopes but also within biotopes Fig. This figure also highlights that, although there was a continuous variation in prokaryote OTU richness among samples, there appear to be high and low diversity host species, in addition to host species of intermediate diversity. Species hosting some of the richest prokaryote communities included the sea cucumber H. In contrast, some of the least diverse prokaryote communities were found in the soft coral Cladiella sp. Species of intermediate diversity included the sponge E.
The large standard deviations in richness values within species, particularly in high diversity hosts, highlights that there was also substantial variation within host species. Certain species also deviated from the general trend of increasing richness and evenness.
Diversity components and distribution of OTUs among biotopes. For example, 1. In this subset, only a very small percentage 1. Of the 21 OTUs restricted to a single biotope, all except three restricted to the sea cucumber mantle were only found in sponges. Thirty-four of the 48 OTUs restricted to two biotopes were also found in sponges and another biotope. The 21 OTUs restricted to a single biotope, give us a new look into the rare members of the coral reef prokaryote metacommunity.
The total abundance of those OTUs varied from 0. OTUs and were restricted to the sponge and sediment biotopes while OTU was restricted to the sea cucumber and nudibranch gut biotopes.
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In Fig. To explore this further, we assessed the number of OTUs shared among biotopes Fig. All but 4 OTUs These five biotopes shared OTUs , while 2 OTUs were only found in sediment, 0 in algae, 9 in the nudibranch mantle, 32 in sponges and 46 in the sea cucumber gut. Note that these OTUs may be present in other biotopes.
Sponges shared 59 OTUs with sediment, which were not shared with the other biotopes compared to 9 OTUs shared between sediment and the sea cucumber gut. Note that just three biotopes, namely, the sea cucumber gut, sponges and nudibranch mantle encompassed all but 6 OTUs Significantly more sediment OTUs were recorded in algae, chitons, stony corals and the sea cucumber gut and mantle than all other biotopes with the exception of the sponge denizen and sea urchin biotopes Fig.
This also held as a percentage of total OTUs Fig. The number of seawater OTUs was highest in the algae and chiton biotopes and significantly more so than in the nudibranch gut and mantle, sponge and soft coral biotopes Fig. Algae, chitons, stony corals and the sea cucumber gut and mantle also housed significantly more environmental OTUs than the nudibranch gut and mantle, flatworm, soft coral and sponge biotopes Fig.
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However, the percentage of environmental OTUs was significantly higher in sponges than all other biotopes, except chitons Fig. Sponges housed a mean of Four of the most abundant OTUs in flatworms OTUs 33, 40, and and two in soft corals OTUs 14 and 17 were only found in host-associated biotopes and were not found in seawater or sediment, explaining the low percentages of environmental sequences in both biotopes Fig.
Mean counts and percentages of sediment, seawater and environmental OTUs in selected hosts. For the HMA sponges, However, sponges may also seed the abiotic environment with their prokaryote symbionts.here
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The present study revealed pronounced differences in composition and diversity among host-associated biotopes. Despite the prevalence of environmental OTUs in sponges, there was pronounced compositional variation between sponges and other host taxa and among sponge species. Certain species, for example, housed prokaryote communities similar to seawater LMA sponges while others HMA sponges housed communities similar to those found in certain samples of nudibranchs and sponge denizens. A number of studies have previously remarked on the greater compositional similarity of the prokaryote communities of HMA as opposed to LMA sponges and the greater prevalence of transient seawater bacteria in the latter 21 , 22 , 23 , LMA sponges have also been shown to be dominated by different sets of highly abundant OTUs and sometimes even a single dominant OTU 8 , 15 , 16 , 25 , 26 , 27 , Compare this to the prokaryote communities of the HMA sponge species X.
The greater evenness of HMA sponge species observed in the present study and other studies may help to explain the greater similarity and limited prevalence of transient bacteria in these sponges Importantly, species evenness has been shown to be positively related to invasion resistance, presumably by limiting the invaders access to available resources The question remains, however, as to why HMA sponges house more even and compositionally similar prokaryote communities than LMA sponges.
Previous studies have shown that certain sponge species are able to transmit microorganisms through their larvae vertical transmission and suggested that this plays an important role in structuring the prokaryote community 3 , 31 , Other studies have focused on horizontal transmission, e. The actual degree to which the sponge prokaryote community is shaped by both forms of transmission, however, remains largely unknown. The compositional similarity between certain sponge samples and samples of nudibranchs and sponge denizens suggests that sponges may influence the prokaryote composition of organisms that live on or within them or that feed on them.
The sponge denizen biotope included sea cucumbers and barnacles that lived within or on the sponge, presumably for much of their life 35 , Nudibranchs, however, are more mobile and may represent vectors carrying microorganisms from one sponge to the other.
Nudibranchs also come into intimate contact with their sponge prey during feeding whereby certain species evert and extend their pharyngeal bulb deep into the sponge During this process, they are also able to sequester toxins from the sponge for their own defence All of these nudibranch species have been recorded feeding on sponges 37 , 39 , 40 , A number of these specimens were also collected from sponges while diving. Specimens of the sea cucumber Synaptula sp. They have also been shown to be able to exploit sponge exudates Interestingly, the barnacle Acasta sp.
The other sponge barnacles were collected within samples of the sponge species Dasychalina fragilis , Agelas cavernosa and Cinachyrella sp.
The similarity between the prokaryote communities of sponges and the guts of certain nudibranch samples, may be an indication that the nudibranch gut communities are dominated by transient microorganisms derived from their preferred food source, namely sponges 37 , This difference can extend to species, whereby there are marked differences in gut microbiome composition among mammal species with different diets 44 , This distinction appears to apply to nudibranchs, whereby the gut and mantle prokaryote communities of species known to feed on sponges closely resembled that of certain sponge species Fig.
It would be interesting to test how different diets e. In line with this, the very high richness and evenness of sediment suggest that it may function as a microbial seed bank. There was also considerable compositional similarity between sediment samples and high diversity host samples of algae, stony corals and sea cucumbers among others. In contrast, seawater samples were only compositionally similar to samples of certain sponge species. Gibbons et al. In their scenario, all microbes are found everywhere due to the immensity and persistence of this seed bank, and apparent local or host-associated endemism is merely a result of insufficient sequencing.
Community structure is, thus, a function of relative abundance rather than the presence or absence of certain microbial taxa. The presence of such a seed bank has repercussions for ecological theory, given the limited importance of long-distance dispersal and the ability of low abundance populations to rapidly expand when the appropriate environment is encountered In the global marine environment, hydrographic parameters of seawater masses, furthermore, greatly contribute to the dispersion of sediment microbial communities at regional and global scales, although microbial cell dispersion is highly dependent on the ability to tolerate stress 49 , Although wide in scope, the present study only represents a small fraction of marine species in the coral reef environment and even in this dataset, there was considerable variation among species within biotopes.
Much more research is needed to understand the variation in microbial composition of taxa such as sea cucumbers, flatworms, algae and nudibranchs. A large amount of time and resources have been spent studying the prokaryote communities of a limited number of taxa leaving large gaps in our knowledge of the coral reef metacommunity. In coral reefs, sponges do not appear to stand alone as the main contributors to total prokaryote diversity as this study highlights; other biotopes host more diverse prokaryote communities, e.
The present study shows that sponges are only one, albeit an interesting, component of a much larger coral reef metacommunity.
All locations were coral reef habitat. A detailed description of the Taiwanese sampling sites can be found in Coelho et al.
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Fragments of host individuals were collected using SCUBA diving, or snorkelling, including the surface and interior or the whole organism depending on the size in order to sample as much as possible of the whole prokaryote community. A total of samples belonging to algae, chitons, stony corals, sea cucumbers, sponge denizens organisms that live on or within sponges , nudibranchs, flatworms, soft corals, sponges, sea urchins, water and sediment were collected.
In the present study, all samples were assigned to 14 biotopes, which included the guts and mantles of sea cucumbers and nudibranchs as separate biotopes. Certain biotopes were well represented, e. A blank control, in which no tissue was added to the Lysing Matrix E tubes, was also included. Multiple samples were pooled together in equal proportions based on their molecular weight and DNA concentrations. Pooled samples were purified using calibrated Ampure XP beads. For a detailed description of the sequence analysis, see Coelho et al.
Default arguments were used except for the minimum sequence length, which was set at base pairs bps after removal of forward primers and barcodes. Potential contaminants were removed from the OTU table if they occurred at least two times in the blank control.
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This conservative measure was chosen because of observations of bleeding between samples from Illumina sequencing and the appearance of abundant reads in blank controls with very low counts 56 , OTUs not classified as Bacteria or Archaea or classified as chloroplasts and mitochondria were also removed. A data matrix containing OTU counts per sample was imported into R using the read. This table was used to compare community composition, estimate richness and assess the relative abundance of selected higher taxa and is included as a Source Data file.
The Bray—Curtis index is one of the most frequently applied dis similarity indices used in ecology 60 , 61 , 62 , Variation in prokaryote composition among biotopes was assessed with Principal Coordinates Analysis PCO using the cmdscale function in R with the Bray—Curtis distance matrix as input. Variation among biotopes was tested for significance using the adonis function in vegan. In the adonis analysis, the Bray—Curtis distance matrix of species composition was the response variable with biotope as independent variable.
The number of permutations was set at ; all other arguments used the default values set in the function.
Weighted average scores were computed for OTUs on the first four PCO axes using the wascores function in the vegan package. The discriminating OTUs contribute the most to differences between pairs of biotopes. We tested for significant differences in the relative abundance of 18 of the most abundant phyla, the four most abundant proteobacterial classes, and the count and relative abundance of sediment and environmental OTUs among biotopes with an analysis of deviance using the glm function in R.
For the most abundant phyla, proteobacterial classes, and the relative abundance of sediment and environmental OTUs, we first applied a generalized linear model GLM with the family argument set to binomial. The ratio, however, of residual deviance to residual d.
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