Abstract

Photosymbiotic protists contribute to surface primary production in low-nutrient, open-ocean ecosystems and constitute model systems for studying plastid acquisition via endosymbiosis. Little is known, however, about host-symbiont dynamics in these important relationships, and whether these symbioses are mutualistic is debated. In this study, we applied single-cell sequencing methods and advanced fluorescent microscopy to investigate host-symbiont dynamics in clade F acantharians, a major group of photosymbiotic protists in oligotrophic subtropical gyres. We amplified the 18S rRNA gene from single acantharian hosts and environmental samples to assess intra-host symbiont diversity and to determine whether intra-host symbiont community composition directly reflects the available symbiont community in the surrounding environment. Our results demonstrate that clade F acantharians simultaneously host multiple species from the haptophyte genera Phaeocystis and Chrysochromulina. The intra-host symbiont community composition was distinct from the external free-living symbiont community, suggesting that these acantharians maintain symbionts for extended periods of time. After selectively staining digestive organelles, fluorescent confocal microscopy showed that symbionts were not being systematically digested, which is consistent with extended symbiont maintenance within hosts. Extended maintenance within hosts may benefit symbionts through protection from grazing or viral lysis, and therefore could enhance dispersal, provided that symbionts retain reproductive capacity. The evidence for extended symbiont maintenance therefore allows that Phaeocystis could glean some advantage from the symbiosis and leaves the possibility of mutualism.

Highlights

  • Photosymbiosis, a nutritional symbiosis where a heterotroph hosts photosynthetic endosymbionts, substantially increases surface primary production in oligotrophic marine ecosystems (Not et al, 2016)

  • 72–99% of sequences were classified as Rhizaria and 1–17% of sequences were classified as Prymnesiophyceae and designated as deriving from symbionts (Supplementary Figure S4)

  • The majority of symbiotic Sequence Variant (SV) in acantharians collected from the East China Sea (ECS) belonged to the Phaeocystis clades cordata, jahnii and Phaeo2, and only 3 of these samples contained SVs belonging to Chrysochromulina

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Summary

Introduction

Photosymbiosis, a nutritional symbiosis where a heterotroph hosts photosynthetic endosymbionts, substantially increases surface primary production in oligotrophic marine ecosystems (Not et al, 2016). Photosymbioses have traditionally been considered mutualisms under the assumption that hosts provide nitrogen to symbionts and symbionts provide organic carbon to hosts in return (Garcia and Gerardo, 2014). Whether these relationships are truly mutualistic or are instead cases of symbiont exploitation has been increasingly questioned in recent years and there is mounting evidence that exploitation is the rule rather than the exception (Keeling and McCutcheon, 2017). Determining the nature of photosymbioses is interesting, as it could provide insight into how the relationships evolve and persist

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