Host-dependent nitrogen recycling as a mechanism of symbiont control in Aiptasia

Abstract

The metabolic symbiosis with photosynthetic algae allows corals to thrive in the oligotrophic environments of tropical seas. Different aspects of this relationship have been investigated using the emerging model organism Aiptasia . However, many fundamental questions, such as the nature of the symbiotic relationship and the interactions of nutrients between the partners remain highly debated. Using a meta-analysis approach, we identified a core set of 731 high-confidence symbiosis-associated genes that revealed host-dependent recycling of waste ammonium and amino acid synthesis as central processes in this relationship. Subsequent validation via metabolomic analyses confirmed that symbiont-derived carbon enables host recycling of ammonium into nonessential amino acids. We propose that this provides a regulatory mechanism to control symbiont growth through a carbon-dependent negative feedback of nitrogen availability to the symbiont. The dependence of this mechanism on symbiont-derived carbon highlights the susceptibility of this symbiosis to changes in carbon translocation, as imposed by environmental stress.

Free‐living and symbiotic lifestyles of a thermotolerant coral endosymbiont display profoundly distinct transcriptomes under both stable and heat stress conditions

“…Longstanding work has shown that symbionts in hospite are generally nitrogen limited as studies have demonstrated that supplemental ammonium increases symbiont density (e.g., Falkowski, Dubinsky, Muscatine, & McCloskey, 1993;Muller-Parker, McCloskey, Hoegh-Guldberg, & McAuley, 1994;Muscatine, Falkowski, Dubinsky, Cook, & McCloskey, 1989), photosynthesis, and chlorophyll content (Hoegh-Guldberg & Smith, 1989), suggesting nitrogen limitation controls symbiont proliferation. Recent work by Cui et al (2019) integrating metabolomics and transcriptomics not only supports this but further suggests that under heat stress, decreased ammonium assimilation by the host results in more ammonium availability to the symbiont, leading to increased symbiont division and the intensification of the disturbance between the two partners.…”

The past, present, and future of coral heat stress studies

“…A growing understanding of the metabolic hostsymbiont relationship has encouraged the use of methods that allow the measuring of these dynamics, such as metabolomics (Cui et al, 2019;Matthews et al, 2017) or NanoSIMS (Krueger et al, 2018). Recent studies have increasingly been combining coral and Symbiodiniaceae responses in their hypothesis testing.…”

“…Recent studies have increasingly been combining coral and Symbiodiniaceae responses in their hypothesis testing. A growing understanding of the metabolic hostsymbiont relationship has encouraged the use of methods that allow the measuring of these dynamics, such as metabolomics (Cui et al, 2019;Matthews et al, 2017) or NanoSIMS (Krueger et al, 2018). These have shown that the metabolic balance between the two partners is not only sensitive to environmental stressors but specifically fine-tuned (Cui et al, 2019;Matthews et al, 2017;Nielsen, Petrou, & Gates, 2018).…”

“…A growing understanding of the metabolic hostsymbiont relationship has encouraged the use of methods that allow the measuring of these dynamics, such as metabolomics (Cui et al, 2019;Matthews et al, 2017) or NanoSIMS (Krueger et al, 2018). These have shown that the metabolic balance between the two partners is not only sensitive to environmental stressors but specifically fine-tuned (Cui et al, 2019;Matthews et al, 2017;Nielsen, Petrou, & Gates, 2018). The coral microbiome has also been shown to significantly impact the thermal stress response mechanisms of the coral as well as on their symbionts (Littman et al, 2010;Pogoreutz et al, 2018;Ziegler et al, 2017).…”

Trophic ecology of shallow and deep reef-building corals

“…Under elevated seawater temperature, the uptake of both nitrate and ammonium is reduced in some coral species (Godinot et al 2011). Alternatively, because coral hosts and symbionts recycle nitrogen and symbiont autotrophy can be maintained by heterotrophic feeding during elevated seawater temperature (Wang and Douglas 1998;Ezzat et al 2016;Tremblay et al 2016), symbiont δ 15 N values may reflect hostdependent regulation of nitrogen available to the symbiont (Falkowski et al 1993;Cui et al 2018).…”