Redox gradients define the ecological niche of ciliates with denitrifying endosymbionts in anoxic lake waters

TL;DR

This study explores how ciliates with denitrifying bacteria live in low-oxygen lakes and how they help consume nitrate.

Contribution

The study identifies the environmental niche and ecological role of ciliates with denitrifying endosymbionts in anoxic lake waters.

Findings

The ciliate hosts thrive in environments with specific sulfide, oxygen, and nitrate conditions.

These ciliates may significantly contribute to nitrate consumption in Lake Zug.

Symbionts divide in coordination with their hosts, suggesting vertical inheritance.

Abstract

Bacterial endosymbionts of the family Candidatus Azoamicaceae obligately associate with anaerobic ciliates belonging to the class Plagiopylea. The symbionts’ unique role for their host involves anaerobic respiration of nitrate and generation of adenosine triphosphate (ATP), analogous to the role of mitochondria in aerobic eukaryotes. As this symbiosis remains so far uncultured, insights into its functioning have been mainly inferred from environmental metagenomes. Here, we investigated the distribution and environmental role of this symbiosis in the anoxic basins of two freshwater lakes, Zug and Lugano (Switzerland), over a course of several years. We found that the environmental niche of the ciliate host is defined by the combined effects of sulfide, oxygen, and nitrate, the latter of which is essential for the symbiont’s respiratory function. Moreover, the distribution and abundance of ciliates with denitrifying endosymbionts in the water column suggest that they may substantially contribute to nitrate consumption in Lake Zug. Our microscopic analyses further demonstrated a coordinated division of the Ca. Azoamicus ciliaticola symbionts and their ciliate hosts, implying a vertical inheritance of denitrifying symbionts. These observations offer new insights into the evolution of ciliates with denitrifying endosymbionts and their ecological role in oxygen-depleted lake waters.

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