Introduced ascidians harbor highly diverse and host-specific symbiotic microbial assemblages

James S Evans,Susanna López-Legentil,Patrick M Erwin,Noa Shenkar

doi:10.1038/s41598-017-11441-4

James S Evans, Susanna López-Legentil + Show 2 more

Open Access

https://doi.org/10.1038/s41598-017-11441-4

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Abstract

Many ascidian species have experienced worldwide introductions, exhibiting remarkable success in crossing geographic borders and adapting to local environmental conditions. To investigate the potential role of microbial symbionts in these introductions, we examined the microbial communities of three ascidian species common in North Carolina harbors. Replicate samples of the globally introduced species Distaplia bermudensis, Polyandrocarpa anguinea, and P. zorritensis (n = 5), and ambient seawater (n = 4), were collected in Wrightsville Beach, NC. Microbial communities were characterized by next-generation (Illumina) sequencing of partial (V4) 16S rRNA gene sequences. Ascidians hosted diverse symbiont communities, consisting of 5,696 unique microbial OTUs (at 97% sequenced identity) from 44 bacterial and three archaeal phyla. Permutational multivariate analyses of variance revealed clear differentiation of ascidian symbionts compared to seawater bacterioplankton, and distinct microbial communities inhabiting each ascidian species. 103 universal core OTUs (present in all ascidian replicates) were identified, including taxa previously described in marine invertebrate microbiomes with possible links to ammonia-oxidization, denitrification, pathogenesis, and heavy-metal processing. These results suggest ascidian microbial symbionts exhibit a high degree of host-specificity, forming intimate associations that may contribute to host adaptation to new environments via expanded tolerance thresholds and enhanced holobiont function.

Highlights

Many ascidian species have experienced worldwide introductions, exhibiting remarkable success in crossing geographic borders and adapting to local environmental conditions
6,372 operational taxonomic units (OTUs) were recovered from Distaplia bermudensis (n = 1,935), Polyandrocarpa anguinea (n = 3,112), P. zorritensis (n = 4,500), and ambient seawater (n = 2,979, Fig. 1)
Half of these OTUs (45%, n = 2,888) were exclusively detected in one source: seawater (n = 676), D. bermudensis (n = 283), P. anguinea (n = 548), or P. zorritensis (n = 1,381) (Fig. 1). 881 OTUs were shared by all four sources, 1,097 OTUs were shared by all three ascidian species, and 3,393 OTUs were recovered from one or more ascidian species and not present in the seawater (Fig. 1)

Summary

Introduction

Many ascidian species have experienced worldwide introductions, exhibiting remarkable success in crossing geographic borders and adapting to local environmental conditions. 103 universal core OTUs (present in all ascidian replicates) were identified, including taxa previously described in marine invertebrate microbiomes with possible links to ammonia-oxidization, denitrification, pathogenesis, and heavy-metal processing These results suggest ascidian microbial symbionts exhibit a high degree of host-specificity, forming intimate associations that may contribute to host adaptation to new environments via expanded tolerance thresholds and enhanced holobiont function. Ascidian larvae are short-lived, non-feeding, and capable of swimming only short distances, while adults are sessile, benthic filter feeders[6] Despite their limited dispersal potential, many ascidian species have been successfully introduced around the world, and rank among the taxa with the highest recorded numbers of introduced species[7,8]. This results in a significant increase in ascidian populations within the afflicted region, often at the expense of the native benthos[21]

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