Insights into the metabolic functioning of a multipartner ciliate symbiosis from oxygen‐depleted sediments

Abstract

Symbioses between anaerobic or microaerophilic protists and prokaryotes are common in anoxic and oxygen-depleted habitats ranging from marine sediments to gastrointestinal tracts. Nevertheless, little is known about the mechanisms of metabolic interaction between partners. In these putatively syntrophic associations, consumption of fermentative end products (e.g., hydrogen) by the prokaryotic symbionts is thought to facilitate protistan anaerobic metabolism. Here, we employed metagenomic and metatranscriptomic sequencing of a microaerophilic or anaerobic karyorelictid ciliate and its prokaryotic symbionts from oxygen-depleted Santa Barbara Basin (CA, USA) sediments to assess metabolic coupling within this consortium. This sequencing confirmed the predominance of deltaproteobacterial symbionts from the Families Desulfobacteraceae and Desulfobulbaceae and suggested active symbiont reduction of host-provided sulphate, transfer of small organic molecules from host to symbionts and hydrogen cycling among the symbionts. In addition, patterns of gene expression indicated active cell division by the symbionts, their growth via autotrophic processes and nitrogen exchange with the ciliate host. Altogether, this research underscores the importance of symbiont metabolism to host fermentative metabolism and, thus, likely its success in anoxic and low-oxygen habitats, but also suggests ciliate-associated prokaryotes play a role in important biogeochemical processes.

Coral-Associated Viral Assemblages From the Central Red Sea Align With Host Species and Contribute to Holobiont Genetic Diversity

“…Coral metagenomes and metatranscriptomes are challenging due to pervasive coral host representation and high and heterogenous sequence diversity that only favors the assembly of the most abundant representatives from the total community, while at the same time it limits the resolution of the compartments with lower biomass such as bacteria and viruses. On the other hand, read-based approaches are proven to be effective to create accurate taxonomical and functional profiles from complex environments where it is not always feasible to produce high quality metagenomes or metatranscriptomes (Beinart et al, 2018;Liu et al, 2019). Here we used the maximum exact match at the protein level as implemented in Kaiju for annotation (Menzel et al, 2016).…”

Enrichment of intracellular sulphur cycle –associated bacteria in intertidal benthic foraminifera revealed by 16S and aprA gene analysis

“…For example, SOB symbionts can fix carbon autotrophically while deriving energy from sulphur-oxidation, and provide the host with organic carbon sources 17 . Sulphur-oxidizing symbioses have been discovered in marine sponges 39 , nematodes 44 , ciliates 18,45,46 and oligochaete worms 36,47 . In turn, SRB symbionts can produce sulphide by oxidizing either organic compounds e.g.…”

“…Endosymbiotic relationships are also common in other marine eukaryotes, offering them potential evolutionary benefits, as they help the host to adapt to unstable conditions and survive in unfavourable environments 17 . For example, ciliates are known to harbour a variety of endobionts linked to carbon, nitrogen and sulphur cycles, which are crucial for the survival of the host species 16,18 . In ciliates, the endosymbiotic relationships are known to have developed independently and species-specifically, and they persisted on long geological time scales 19 .…”

Editorial 2019

“…The first section focused on the mechanistic underpinnings of host-microbe interactions, all the way from obligate symbioses where nutritional codependence is common (Beinart, Beaudoin, Bernhard, & Edgcomb, 2018;Feng, Wang, Wuchty, & Wilson, 2018;Thairu, Cheng, & Hansen, 2018), to more transient ones where benefits can include defence, growth and development, and tolerance to abiotic stress (Bost et al, 2018;Haney et al, 2018;Hudson, Gardiner, Deshpande, & Egan, 2018;Kessler, Weiss, Kuegler, Hermes, & Wichard, 2018;Palakurty, Stinchcombe, & Afkhami, 2018).…”