Testing assumptions of nitrogen cycling between a temperate, model coral host and its facultative symbiont: symbiotic contributions to dissolved inorganic nitrogen assimilation

Le Diroberts,A Dudek,Rw Fulweiler,Rd Rotjan,Ne Ray

doi:10.3354/meps13731

Abstract

Coral symbioses are predicated on the need for mutual nutrient acquisition and translocation between partners. Carbon translocation is well-studied in this classic mutualism, while nitrogen (N) has received comparatively less attention. Quantifying the mechanisms and dynamics of N assimilation is critical to understanding the functional ecology of coral organisms. Given the importance of symbiosis to the coral holobiont, it is important to determine what role photosynthetic symbionts play in N acquisition. We used the facultatively symbiotic temperate coral Astrangia poculata and 15N labeling to test the effects of symbiotic state and trophic status on N acquisition. We tracked assimilation of 2 forms of isotopically labeled dissolved inorganic N (DIN: ammonium, 15NH4+ and nitrate, 15NO3-) by fed and starved colonies of both symbiotic and aposymbiotic A. poculata. Coral holobiont tissue was subsequently analyzed for δ15N and changes in photosynthetic efficiency. Results suggest that corals acquired the most N from DIN via their symbiont Breviolum psygmophilum and that NH4+ is more readily assimilated than NO3-. Photosynthetic efficiency increased with the addition of NH4+, but only for fed, symbiotic treatments. NO3- adversely affected photosynthetic efficiency among starved corals. Our results suggest that symbiosis is advantageous for DIN acquisition, that dysbiosis inhibits corals’ mixotrophic strategy of nutrient acquisition, and that either feeding or symbiosis alone does not fully provide the energetic advantage of both. This study lends support to the emerging hypothesis that symbionts are mutualists in optimal conditions but shift to a parasitic paradigm when resources or energy are scarce.

Highlights

Mixotrophy, the derivation of nourishment from both autotrophy and heterotrophy, is common among symbiotic marine organisms
Coral symbioses are predicated on the need for mutual nutrient acquisition and translocation between partners (Muscatine & Porter 1977, Tremblay et al 2012, 2014)
The aim of this study was to explore nutrient acquisition pathways in corals and their symbionts under several N-availability, symbiotic state, and heterotrophy/autotrophy scenarios. This experiment answers 4 key mechanistic, ecologically relevant functional questions: (1) natural abundance δ15N values are higher in aposymbiotic colonies of wild-collected Astrangia poculata than in symbiotic colonies; (2) NH4+ is more readily assimilated than NO3− by both symbiotic and aposymbiotic colonies; (3) there is no evidence of compensatory nutrient uptake in the absence of heterotrophy, instead, fed corals are more able to absorb and utilize N; and (4) enhanced dissolved inorganic N (DIN) assimilation is associated with greater photosynthetic efficiency for NH4+

Summary

Introduction

Mixotrophy, the derivation of nourishment from both autotrophy and heterotrophy, is common among symbiotic marine organisms. Symbiotic hosts either draw upon nutrient reserves (Fitt et al 1993, Schoepf et al 2015, Levas et al 2018) or shift to increased heterotrophy during periods of stress (Palardy et al 2005, 2008, Grottoli et al 2006, reviewed by Houlbrèque & Ferrier-Pagès 2009) These triage behaviors are not sustainable in the long term (Grottoli et al 2006) as most tropical corals have an obligate relationship with their symbionts wherein up to 95% of autotrophically fixed C is translocated from the symbiont to the host (McCloskey & Muscatine 1984, Muscatine et al 1984, Davies 1991, Davy et al 1996, Alamaru et al 2009, Bednarz et al 2017)

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