Bacterial symbiont subpopulations have different roles in a deep-sea symbiosis.

Tjorven Hinzke,Horst Felbeck,Rabea Schlüter,Thomas Schweder,Uwe Völker,Manuel Kleiner,Stephanie Markert,Stefan M Sievert,Dörte Becher,Florian Bonn,Mareike Meister,Petra Hildebrandt,Jan Pané-Farré,Christian Hentschker

doi:10.7554/elife.58371

Abstract

The hydrothermal vent tubeworm Riftia pachyptila hosts a single 16S rRNA phylotype of intracellular sulfur-oxidizing symbionts, which vary considerably in cell morphology and exhibit a remarkable degree of physiological diversity and redundancy, even in the same host. To elucidate whether multiple metabolic routes are employed in the same cells or rather in distinct symbiont subpopulations, we enriched symbionts according to cell size by density gradient centrifugation. Metaproteomic analysis, microscopy, and flow cytometry strongly suggest that Riftia symbiont cells of different sizes represent metabolically dissimilar stages of a physiological differentiation process: While small symbionts actively divide and may establish cellular symbiont-host interaction, large symbionts apparently do not divide, but still replicate DNA, leading to DNA endoreduplication. Moreover, in large symbionts, carbon fixation and biomass production seem to be metabolic priorities. We propose that this division of labor between smaller and larger symbionts benefits the productivity of the symbiosis as a whole.

Highlights

The chemoautotrophic gammaproteobacterium Candidatus Endoriftia persephone, sulfur-oxidizing endosymbiont of the deep-sea tubeworm Riftia pachyptila, provides all nutrition for its gutless host (Cavanaugh et al, 1981; Felbeck, 1981; Hand, 1987; Robidart et al, 2008)
The enrichment procedure was highly reproducible, for symbionts isolated from sulfur-rich trophosome tissue (Figure 1)
Amongst a number of particle groups with different properties, we found two populations, 1 and 2, which were abundantly detected in nonenriched trophosome homogenate, but showed very dissimilar frequencies in fractions enriched in larger or smaller symbionts (Figure 2, Figure 2—figure supplement 1): While population 1, which exhibited relatively lower Forward scatter (FSC) and side scatter (SSC) signals, was highly abundant in fractions enriched in smaller symbionts, this population was notably less prominent in fractions enriched in larger symbionts

Summary

Introduction

The chemoautotrophic gammaproteobacterium Candidatus Endoriftia persephone, sulfur-oxidizing endosymbiont of the deep-sea tubeworm Riftia pachyptila (here Riftia), provides all nutrition for its gutless host (Cavanaugh et al, 1981; Felbeck, 1981; Hand, 1987; Robidart et al, 2008). Ca. E. persephone (here Endoriftia) densely populates Riftia’s trophosome, a specialized organ in the worm’s trunk, where the bacteria are housed intracellularly in host bacteriocytes (Hand, 1987). Fueled by the oxidation of reduced sulfur compounds (mainly sulfide), the symbionts fix CO2 and produce considerable amounts of biomass, which constitutes the host’s source of nutrition

Objectives

Methods

Results

Discussion

Conclusion