Photosymbiosis in Late Triassic scleractinian corals from the Italian Dolomites

Abstract

During the Carnian, oligotrophic shallow-water regions of the western Tethys were occupied by small, coral-rich patch reefs. Scleractinian corals, which already contributed to the formation of the reef structure, owed their position most probably to the symbiosis with dinoflagellate algae (zooxanthellae). Using microstructural (regularity of growth increments) and geochemical (oxygen and carbon stable isotopes) criteria of zooxanthellae symbiosis, we investigated whether this partnership was widespread among Carnian scleractinians from the Italian Dolomites (locality Alpe di Specie). Although corals from this locality are renowned from excellent mineralogical preservation (aragonite), their skeletons were rigorously tested against traces of diagenesis Irrespective of their growth forms, well preserved skeletons of corals from the Dolomites, most frequently revealed regular growth bands (low values of coefficient of variation) typical of modern zooxanthellate corals. Paradoxically, some Carnian taxa (Thamnasteriomorpha frechi and Thamnasteriomorphasp.)with highly integrated thamnasterioid colonies which today are formed exclusively by zooxanthellate corals, showed irregular fine-scale growth bands (coefficient of variation of 40% and 41% respectively) that could suggest their asymbiotic status. However, similar irregular skeletal banding is known also in some modern agariciids (Leptoseris fragilis) which are symbiotic with zooxanthellae. This may point to a similar ecological adaptation of Triassic taxa with thamnasterioid colonies. Contrary to occasionally ambiguous interpretation of growth banding, all examined Carnian corals exhibited lack of distinct correlation between carbon (δ13C range between 0.81‰ and 5.81‰) and oxygen (δ18O values range between −4.21‰ and −1.06‰) isotope composition of the skeleton which is consistent with similar pattern in modern zooxanthellates. It is therefore highly likely, that Carnian scleractinian corals exhibited analogous ecological adaptations as modern symbiotic corals and that coral-algal symbiosis that spread across various clades of Scleractinia preceded the reef bloom at the end of the Triassic.

Massive genome reduction occurred prior to the origin of coral algal symbionts

“…Common and distinct genomic features we observed between early and late-branching symbiotic lineages of Symbiodiniaceae suggest an interplay between the geological eras during which they arose, and the corresponding coral morphology and ocean chemistry (Figure 6). Ancestral Symbiodiniaceae started inhabiting stony corals presumably as early as 230 MYA in the late Triassic (Frankowiak et al 2021) and may have driven the Norian-Rhaetian reef bloom (Kiessling et al 2009). These early Scleractinian corals (e.g., Retiophyllia ) tended to be uniserial, i.e., possessing one corallite per branch, and phaceloid with thick walls (Coates and Jeremy 1987; Stanley 2003), and thus were less efficient at harvesting light (Enríquez et al 2017).…”

“…Of particular importance to modern coral reefs, these dinoflagellates provide photosynthates via fixed carbon and essential nutrients to corals while resident in these cnidarians. The Symbiodiniaceae ancestor is believed to have been freeliving (LaJeunesse et al 2018) with members of this group forming symbiotic associations with corals as early as 230 million years ago (MYA) (Frankowiak et al 2021).…”

“…Based on current divergence time estimates for Symbiodiniaceae, the split between the basal genera (Symbiodinium and Philozoon) and the rest of the family occurred 166 MYA, whereas the more-recently branching symbiotic lineages diversified ~109 MYA (LaJeunesse et al 2018). If the emergence of symbiogenesis coincides with the earliest fossil evidence from 230 MYA (Frankowiak et al 2021), then different Symbiodiniaceae lineages would have arose and diversified during major global geological events. These events include the switch from aragonite to calcite seas (~190 MYA (Vulpius and Kiessling 2017)), the breakup of Pangea (150-230 MYA (Schettino and Turco 2009)), the diversification or extinction of potential hosts, e.g., the extinction of rudists 66 MYA (Stanley and van de Schootbrugge 2018;de Winter et al 2020), and the overall change in coral morphology from the Triassic (201-252 MYA) to the Cretaceous (66-145 MYA) (Veron 2011;Pandolfi and Kiessling 2014).…”

“…Of particular importance to modern coral reefs, these dinoflagellates provide photosynthates via fixed carbon and essential nutrients to corals while resident in these cnidarians. The Symbiodiniaceae ancestor is believed to have been free-living (LaJeunesse et al 2018) with members of this group forming symbiotic associations with corals as early as 230 million years ago (MYA) (Frankowiak et al 2021). Symbiogenesis, or the establishment of a symbiotic relationship between two or more taxa (Guerrero et al 2013), can drastically influence their evolution, adaptation, and speciation as observed in obligate parasites and diverse symbiotic taxa (Stephen et al 2005; Morrison et al 2007; Opperman et al 2008; Kwan et al 2012; McCutcheon and Moran 2012).…”

Acclimatization of a coral-dinoflagellate mutualism at a CO2 vent

“…The symbiosis between scleractinian corals and their dinoflagellate microalgae (family Symbiodiniaceae), commonly referred to as zooxanthellae, has been extensively studied [15][16][17] . Zooxanthellae significantly contribute to the energy budget of the host by providing photosynthetically fixed carbon 16 while recycling host respiration and excretion by-products 18 .…”