The trace metal economy of the coral holobiont: supplies, demands and exchanges

Abstract

The juxtaposition of highly productive coral reef ecosystems in oligotrophic waters has spurred substantial interest and progress in our understanding of macronutrient uptake, exchange, and recycling among coral holobiont partners (host coral, dinoflagellate endosymbiont, endolithic algae, fungi, viruses, bacterial communities). By contrast, the contribution of trace metals to the physiological performance of the coral holobiont and, in turn, the functional ecology of reef‐building corals remains unclear. The coral holobiont's trace metal economy is a network of supply, demand, and exchanges upheld by cross‐kingdom symbiotic partnerships. Each partner has unique trace metal requirements that are central to their biochemical functions and the metabolic stability of the holobiont. Organismal homeostasis and the exchanges among partners determine the ability of the coral holobiont to adjust to fluctuating trace metal supplies in heterogeneous reef environments. This review details the requirements for trace metals in core biological processes and describes how metal exchanges among holobiont partners are key to sustaining complex nutritional symbioses in oligotrophic environments. Specifically, we discuss how trace metals contribute to partner compatibility, ability to cope with stress, and thereby to organismal fitness and distribution. Beyond holobiont trace metal cycling, we outline how the dynamic nature of the availability of environmental trace metal supplies can be influenced by a variability of abiotic factors (e.g. temperature, light, pH, etc.). Climate change will have profound consequences on the availability of trace metals and further intensify the myriad stressors that influence coral survival. Lastly, we suggest future research directions necessary for understanding the impacts of trace metals on the coral holobiont symbioses spanning subcellular to organismal levels, which will inform nutrient cycling in coral ecosystems more broadly. Collectively, this cross‐scale elucidation of the role of trace metals for the coral holobiont will allow us to improve forecasts of future coral reef function.

Nutritional exchange between reef-building corals and algal endosymbionts buffers the energetic demand of larval development and metamorphosis

“…In late development, the relative abundance of Rhodobacteraceae and Flavobacteriaceae increases (SI Appendix, Fig S3CD). These taxa play a role in carbon (43), nitrogen (41), sulfur (e.g., DMSP/DMS; (44), and micronutrient cycling (45) along with the production of antimicrobial compounds (46) and, therefore, we hypothesize that an increase in bacterial diversity could confer increased nutritional functional diversity for the host (47, 48). Quantitative measures of nutritional production and cycling in bacterial communities across ontogeny should be completed in future studies with approaches such as metatranscriptomics, DNA-stable isotope probing (e.g., DNA-SIP), as well as metabolomic stable isotope probing and microscopy techniques (e.g., NanoSIMS) to test this hypothesis (49).…”

A Perspective on Probing Coral Resilience to Climate and Environmental Changes Using Stable Isotopes of Bio‐Utilized Metal Elements

“…This integrated approach is fundamental for accurately interpreting metal stable isotopes data, linking the fractionation and composition of metal stable isotopes in corals to the holobiont's biological activities. Delving into the coral holobiont's metal economy, that is, the intricate network of supply, demand, and exchanges driven by symbiotic relationships (Reich et al., 2023), is crucial. Moreover, integrating geochemical, biological, and ecological research across various biological levels of organization is essential.…”

“…These metal elements are integral to their physiological performance, as many enzymes rely on metal‐containing cofactors for activity. The supply, demand, and exchange of these metal elements, maintained through symbiotic partnerships across kingdoms, are essential for core biological processes such as macronutrient uptake and assimilation, photosynthesis, cellular respiration, and nucleic acid metabolism (Reich et al., 2023; Figure 1). For example, while an excess of Cu and Zn can be toxic, these elements are vital for coral growth, forming parts of various enzymes like cytochrome oxidase (Cu, Medeiros and Jennings, 2002) and carbonic anhydrase (Zn, Morel et al., 1994).…”

“…The increased attention to metal stable isotopes stems from the crucial roles of specific metal elements like iron (Fe), copper (Cu), zinc (Zn), molybdenum (Mo), magnesium (Mg), vanadium (V), and cobalt (Co). These metals, acting as essential micronutrients, play integral roles in various processes within coral holobiont symbioses (Figure 1; see Reich et al (2023) for a detailed review), positioning them as potential indicators of coral biological activities. In this light, we contend that leveraging the rapid progress in the study of metal stable isotopes can greatly enhance our understanding of coral biological responses to climate and environmental changes.…”

Contrasting effects of increasing dissolved iron on photosynthesis and O2 availability in the gastric cavity of two Mediterranean corals

“…Scleractinian corals are the foundation species of tropical coral reefs and temperate coralligenous assemblages ( Hoeksema, 2017 ; Ingrosso et al, 2018 ). Their metabolic processes ( i.e., cellular respiration, symbiont photosynthesis, calcification), as well as cellular homeostasis ( Reich et al, 2023 ), are linked to macro- and micro-nutrient availability through host feeding and nutrient uptake by endosymbionts ( Muscatine & Porter, 1977 ; Houlbrèque & Ferrier-Pagès, 2009 ; Houk et al, 2020 ). Among micro-nutrients, iron is fundamental for cellular function and metabolism ( Raven, Evans & Korb, 1999 ; Behrenfeld & Milligan, 2013 ; D’Angelo & Wiedenmann, 2014 ; Reich et al, 2020 ).…”