Abstract
BackgroundArchaea are ubiquitous symbionts of marine sponges but their ecological roles and the influence of environmental factors on these associations are still poorly understood.Methodology/Principal FindingsWe compared the diversity and composition of archaea associated with seawater and with the sponges Hymeniacidon heliophila, Paraleucilla magna and Petromica citrina in two distinct environments: Guanabara Bay, a highly impacted estuary in Rio de Janeiro, Brazil, and the nearby Cagarras Archipelago. For this we used metagenomic analyses of 16S rRNA and ammonia monooxygenase (amoA) gene libraries. Hymeniacidon heliophila was more abundant inside the bay, while P. magna was more abundant outside and P. citrina was only recorded at the Cagarras Archipelago. Principal Component Analysis plots (PCA) generated using pairwise unweighted UniFrac distances showed that the archaeal community structure of inner bay seawater and sponges was different from that of coastal Cagarras Archipelago. Rarefaction analyses showed that inner bay archaeaoplankton were more diverse than those from the Cagarras Archipelago. Only members of Crenarchaeota were found in sponge libraries, while in seawater both Crenarchaeota and Euryarchaeota were observed. Although most amoA archaeal genes detected in this study seem to be novel, some clones were affiliated to known ammonia oxidizers such as Nitrosopumilus maritimus and Cenarchaeum symbiosum.Conclusion/SignificanceThe composition and diversity of archaeal communities associated with pollution-tolerant sponge species can change in a range of few kilometers, probably influenced by eutrophication. The presence of archaeal amoA genes in Porifera suggests that Archaea are involved in the nitrogen cycle within the sponge holobiont, possibly increasing its resistance to anthropogenic impacts. The higher diversity of Crenarchaeota in the polluted area suggests that some marine sponges are able to change the composition of their associated archaeal communities, thereby improving their fitness in impacted environments.
Highlights
Sponges are ancient, sessile, highly efficient filter-feeding animals, with fossils dating back to the Late Precambrian [1]
We demonstrate that each species has a distinct archaeal community and that species displaying diverse archaeal communities survive in the eutrophic environment
Phosphate and ammonium values were an order of magnitude higher within the bay than in the Cagarras Archipelago (Fig. 1B)
Summary
Sessile, highly efficient filter-feeding animals, with fossils dating back to the Late Precambrian [1]. Symbiont microbial communities are likely to have appeared in the same period, sharing a long association history with their sponge hosts [2]. Sponges are among the invertebrate phyla that most commonly harbors associated microbial communities, and some species have even been called ‘‘bacteriosponges’’ due to the high content of bacterial cells in their tissues [3]. These symbiotic relationships occur with a variety of heterotrophic and autotrophic bacteria, archaea, protists and microalgae [2]. Archaea are ubiquitous symbionts of marine sponges but their ecological roles and the influence of environmental factors on these associations are still poorly understood
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