Abstract

The diversity and specificity of microbial communities in marine environments is a key aspect of the ecology and evolution of both the eukaryotic hosts and their associated prokaryotes. Marine sponges harbor phylogenetically diverse and complex microbial lineages. Here, we investigated the sponge bacterial community and distribution patterns of microbes in three sympatric intertidal marine demosponges, Hymeniacidon perlevis, Ophlitaspongia papilla and Polymastia penicillus, from the Atlantic coast of Portugal using classical isolation techniques and 16S rRNA gene clone libraries. Microbial composition assessment, with nearly full-length 16S rRNA gene sequences (ca. 1400 bp) from the isolates (n = 31) and partial sequences (ca. 280 bp) from clone libraries (n = 349), revealed diverse bacterial communities and other sponge-associated microbes. The majority of the bacterial isolates were members of the order Vibrionales and other symbiotic bacteria like Pseudovibrio ascidiaceiocola, Roseobacter sp., Hahellaceae sp. and Cobetia sp. Extended analyses using ecological metrics comprising 142 OTUs supported the clear differentiation of bacterial community profiles among the sponge hosts and their ambient seawater. Phylogenetic analyses were insightful in defining clades representing shared bacterial communities, particularly between H. perlevis and the geographically distantly-related H. heliophila, but also among other sponges. Furthermore, we also observed three distinct and unique bacterial groups, Betaproteobactria (∼81%), Spirochaetes (∼7%) and Chloroflexi (∼3%), which are strictly maintained in low-microbial-abundance host species O. papilla and P. penicillus. Our study revealed the largely generalist nature of microbial associations among these co-occurring intertidal marine sponges.

Highlights

  • Sponges (Phylum Porifera) are an ancient groups of invertebrate metazoans, with a fossil record dating back to 600 million years and with a host of diverse symbiotic microorganisms such as archaea [1], cyanobacteria [2], heterotrophic bacteria [3], algae, fungi [4] and dinoflagellates [5]

  • Additional data on bacterial diversity is needed to better describe sponge-microbe associations and in this study we examined the bacterial diversity in three co-occurring intertidal sponges from the Atlantic Ocean in Portugal: Hymeniacidon perlevis Montagu, 1818 (Halichondrida: Halichondriidae), Ophlitaspongia papilla Bowerbank, 1866 (Poeciosclerida: Microcionidae) and Polymastia penicillus Montagu, 1818 (Hadromerida: Polymastiidae)

  • Culture-dependent techniques allowed the isolation of heterotrophic bacteria from the marine sponges H. perlevis (n = 9), O. papilla (n = 11) and P. penicillus (n = 11)

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Summary

Introduction

Sponges (Phylum Porifera) are an ancient groups of invertebrate metazoans, with a fossil record dating back to 600 million years and with a host of diverse symbiotic microorganisms such as archaea [1], cyanobacteria [2], heterotrophic bacteria [3], algae, fungi [4] and dinoflagellates [5]. A new model of symbiont acquisition that includes both larval-mediated transfer and environmental uptake in the formation of complex sponge microbiota has been proposed [10]. Diverse sponge microbiota may contribute to the host’s metabolism with photosynthesis [2], major nitrogen cycle events [11,12,13,14], sulfate reduction [15] and carbon fixation [16,17] and in return, the host provides an enriched ecological niche for its microbial partners.

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