Host-specific symbioses and the microbial prey of a pelagic tunicate (Pyrosoma atlanticum)

Anne W Thompson,Anna C Ward,Carey P Sweeney,Kelly R Sutherland

doi:10.1038/s43705-021-00007-1

Anne W Thompson, Anna C Ward + Show 2 more

Open Access

https://doi.org/10.1038/s43705-021-00007-1

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Abstract

Pyrosomes are widely distributed pelagic tunicates that have the potential to reshape marine food webs when they bloom. However, their grazing preferences and interactions with the background microbial community are poorly understood. This is the first study of the marine microorganisms associated with pyrosomes undertaken to improve the understanding of pyrosome biology, the impact of pyrosome blooms on marine microbial systems, and microbial symbioses with marine animals. The diversity, relative abundance, and taxonomy of pyrosome-associated microorganisms were compared to seawater during a Pyrosoma atlanticum bloom in the Northern California Current System using high-throughput sequencing of the 16S rRNA gene, microscopy, and flow cytometry. We found that pyrosomes harbor a microbiome distinct from the surrounding seawater, which was dominated by a few novel taxa. In addition to the dominant taxa, numerous more rare pyrosome-specific microbial taxa were recovered. Multiple bioluminescent taxa were present in pyrosomes, which may be a source of the iconic pyrosome luminescence. We also discovered free-living marine microorganisms in association with pyrosomes, suggesting that pyrosome feeding impacts all microbial size classes but preferentially removes larger eukaryotic taxa. This study demonstrates that microbial symbionts and microbial prey are central to pyrosome biology. In addition to pyrosome impacts on higher trophic level marine food webs, the work suggests that pyrosomes also alter marine food webs at the microbial level through feeding and seeding of the marine microbial communities with their symbionts. Future efforts to predict pyrosome blooms, and account for their ecosystem impacts, should consider pyrosome interactions with marine microbial communities.

Highlights

Pyrosomes are globally abundant pelagic tunicates that can alter marine ecosystems, especially when they bloom
Addressing pyrosome interactions with marine microorganisms could improve the understanding of pyrosome biology, bloom dynamics, and impacts to ecosystems because marine microorganisms are major players in animal biology,[15] marine trophic structure,[16] and biogeochemical cycling.[17]
Pyrosome-specific microbial community This is the first study to report on the microbial communities of invertebrates suggesting that pyrosomes contain unique symbionts

Summary

Introduction

Pyrosomes are globally abundant pelagic tunicates that can alter marine ecosystems, especially when they bloom. Pyrosomes graze efficiently[1,2,3,4,5] and, in turn, become prey to fish,[6,7] sea turtles,[8] seabirds,[9,10] and marine mammals,[11] and provide habitats to invertebrates.[8,12] Through sinking after death, vertical migration, and fecal pellets, pyrosomes contribute to detrital food webs, transport carbon below the mixed layer,[3] and feed benthic megafauna.[13,14] pyrosomes have the capacity to dramatically alter energy and carbon cycles in marine ecosystems, knowledge of pyrosome biology is limited. Pyrosome bioluminescence suggests a hostspecific relationship with microbial symbionts, though none have been identified.[20,21,22] The microbiomes of other tunicates provide their host with nitrogen,[23] carbon,[24] secondary metabolites,[25] extending the host range into nutrient poor environments

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