Multiple bacterial partners in symbiosis with the nudibranch mollusk Rostanga alisae

Natalia V Zhukova,Evgeniy S Balakirev,Marina G Eliseikina,Francisco J Ayala

doi:10.1038/s41598-021-03973-7

Abstract

The discovery of symbiotic associations extends our understanding of the biological diversity in the aquatic environment and their impact on the host’s ecology. Of particular interest are nudibranchs that unprotected by a shell and feed mainly on sponges. The symbiotic association of the nudibranch Rostanga alisae with bacteria was supported by ample evidence, including an analysis of cloned bacterial 16S rRNA genes and a fluorescent in situ hybridization analysis, and microscopic observations. A total of 74 clones belonging to the phyla α-, β-, γ-Proteobacteria, Actinobacteria, and Cyanobacteria were identified. FISH confirmed that bacteriocytes were packed with Bradyrhizobium, Maritalea, Labrenzia, Bulkholderia, Achromobacter, and Stenotrophomonas mainly in the foot and notum epidermis, and also an abundance of Synechococcus cyanobacteria in the intestinal epithelium. An ultrastructural analysis showed several bacterial morphotypes of bacteria in epidermal cells, intestine epithelium, and in mucus layer covering the mollusk body. The high proportion of typical bacterial fatty acids in R. alisae indicated that symbiotic bacteria make a substantial contribution to its nutrition. Thus, the nudibranch harbors a high diversity of specific endo- and extracellular bacteria, which previously unknown as symbionts of marine invertebrates that provide the mollusk with essential nutrients. They can provide chemical defense against predators.

Highlights

The discovery of symbiotic associations extends our understanding of the biological diversity in the aquatic environment and their impact on the host’s ecology
The analysis of the cloned bacterial 16S rRNA genes allowed to obtain the most conservative and reliable scan of bacterial diversity, which made it possible to reveal bacteria that form mutualistic relationships with the host and to formulate the most parsimonious hypothesis concerning the functional importance of the symbiosis
In these cases, symbioses involving bacteria and marine invertebrates are either endosymbiotic microbes co-occurring inside the host b acteriocytes[5,11] or ectosymbiotic microbes associated with the external surfaces of the a nimals[3,4,9,15,34], with the exception of scaly-foot snail from hydrothermal vents having partnerships simultaneously with epi- and endosymbiontic m icrobes[35]

Summary

Introduction

The discovery of symbiotic associations extends our understanding of the biological diversity in the aquatic environment and their impact on the host’s ecology. The nudibranch harbors a high diversity of specific endo- and extracellular bacteria, which previously unknown as symbionts of marine invertebrates that provide the mollusk with essential nutrients. They can provide chemical defense against predators. The discovery of new symbiosis extends our understanding of the symbiotic diversity and their impact on the ecology and evolution of the marine invertebrates. A number of nudibranch species, belonging to two groups, Aeolidoidea and Dendronotoidea, have symbiotic relationships with photosynthetic dinoflagellates They usually acquire them by sequestration from their prey and keep them inside cells of digestive g land[16,17,18].

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Conclusion