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Abstract:
Since the discovery of symbioses between sulfur-oxidizing (thiotrophic)
bacteria and invertebrates at hydrothermal vents over 40 years ago, it
has been assumed that autotrophic fixation of CO2 by the symbionts
drives these nutritional associations. In this study, we investigated
"Candidatus Kentron," the clade of symbionts hosted by Kentrophoros, a
diverse genus of ciliates which are found in marine coastal sediments
around the world. Despite being the main food source for their hosts,
Kentron bacteria lack the key canonical genes for any of the known
pathways for autotrophic carbon fixation and have a carbon stable
isotope fingerprint that is unlike other thiotrophic symbionts from
similar habitats. Our genomic and transcriptomic analyses instead found
metabolic features consistent with growth on organic carbon, especially
organic and amino acids, for which they have abundant uptake
transporters. All known thiotrophic symbionts have converged on using
reduced sulfur to gain energy lithotrophically, but they are diverse in
their carbon sources. Some clades are obligate autotrophs, while many
are mixotrophs that can supplement autotrophic carbon fixation with
heterotrophic capabilities similar to those in Kentron. Here we show
that Kentron bacteria are the only thiotrophic symbionts that appear to
be entirely heterotrophic, unlike all other thiotrophic symbionts
studied to date, which possess either the Calvin-Benson-Bassham or the
reverse tricarboxylic acid cycle for autotrophy.
IMPORTANCE Many animals and protists depend on symbiotic
sulfur-oxidizing bacteria as their main food source. These bacteria use
energy from oxidizing inorganic sulfur compounds to make biomass
autotrophically from CO2, serving as primary producers for their hosts.
Here we describe a clade of nonautotrophic sulfur-oxidizing symbionts,
"Candidatus Kentron," associated with marine ciliates. They lack genes
for known autotrophic pathways and have a carbon stable isotope
fingerprint heavier than other symbionts from similar habitats. Instead,
they have the potential to oxidize sulfur to fuel the uptake of organic
compounds for heterotrophic growth, a metabolic mode called
chemolithoheterotrophy that is not found in other symbioses. Although
several symbionts have heterotrophic features to supplement primary
production, in Kentron they appear to supplant it entirely.
