Revealing changes in the microbiome of Symbiodiniaceae under thermal stress

Abstract

Summary Symbiodiniaceae are a diverse family of marine dinoflagellates, well known as coral endosymbionts. Isolation and in vitro culture of Symbiodiniaceae strains for physiological studies is a widely adopted tool, especially in the context of understanding how environmental stress perturbs Symbiodiniaceae cell functioning. While the bacterial microbiomes of corals often correlate with coral health, the bacterial communities co‐cultured with Symbiodiniaceae isolates have been largely overlooked, despite the potential of bacteria to significantly influence the emergent physiological properties of Symbiodiniaceae cultures. We examined the physiological response to heat stress by Symbiodiniaceae isolates (spanning three genera) with well‐described thermal tolerances, and combined these observations with matched changes in bacterial composition and abundance through 16S rRNA metabarcoding. Under thermal stress, there were Symbiodiniaceae strain‐specific changes in maximum quantum yield of photosystem II (proxy for health) and growth rates that were accompanied by changes in the relative abundance of multiple Symbiodiniaceae‐specific bacteria. However, there were no Symbiodiniaceae‐independent signatures of bacterial community reorganisation under heat stress. Notably, the thermally tolerant Durusdinium trenchii (ITS2 major profile D1a) had the most stable bacterial community under heat stress. Ultimately, this study highlights the complexity of Symbiodiniaceae‐bacteria interactions and provides a first step towards uncoupling their relative contributions towards Symbiodiniaceae physiological functioning.

Intracellular bacteria are common and taxonomically diverse in cultured and in hospite algal endosymbionts of coral reefs

“…We demonstrate that daily cycling and sampling time, especially light, influence the proportion of Symbiodiniaceae cells that are closely associated with bacteria. This is concordant with previous studies that showed Symbiodiniaceae bacterial communities change with temperature [41], and that bacterial density increases with culture age in the dinoflagellates Heterocapsa circularisquama, Alexandrium catenella, and Protoceratium reticulatum [11,80]. It was also shown in H. circularisquama that the density of intracellular bacteria increases when the dinoflagellate culture is switched to continuous darkness [80], an increase we also report here during the night period.…”

“…Metabarcoding data indicated that bacterial communities associated with Symbiodiniaceae cultures were largely comprised of Hyphomicrobium, Methylobacterium, Sphingomonas, Marinobacter, Labrenzia, Balneola, Algiphilus, Rhodobacteraceae, Phycisphaeraeae, and Roseitalea. Marinobacter, Labrenzia, and Muricauda were previously found to be abundant in a wide range of Symbiodiniaceae cultures [39][40][41], indicating the conservation of specific bacterial associates across Symbiodiniaceae species, coral hosts, and coral host location. Marinobacter enhances the growth of Scrippsiella trochoidea, presumably by producing vibrioferrin, a siderophore that promotes iron uptake by the dinoflagellate [18].…”

“…To date, few studies have investigated the microbiome of Symbiodiniaceae [39][40][41]. Lawson et al reported the composition of the bacterial communities associated with 18 Symbiodiniaceae cultures [40].…”

“…Communities were dominated by Alpha-and Gammaproteobacteria with Labrenzia, Marinobacter, and Chromatiaceae found in all cultures. Camp et al studied the impact of a thermal stress event on the bacterial community composition of four Symbiodiniaceae cultures, finding again a high prevalence of Alphaproteobacteria, and particularly Labrenzia [41]. However, neither of these studies distinguished the planktonic bacteria from the bacteria closely associated with the algae.…”

Increased diversity and concordant shifts in community structure of coral‐associated Symbiodiniaceae and bacteria subjected to chronic human disturbance

“…During coral bleaching (the breakdown of the symbiosis between corals and Symbiodiniaceae), coral microbiomes may shift from healthy communities towards opportunistic taxa such as Vibrio (Bourne et al., 2008). Furthermore, a recent in vitro experiment showed that warming caused changes in Symbiodiniaceae culture‐associated bacterial communities, and that compared to Cladocopium C1 and Breviolum sp., the heat‐tolerant Durusdinium trenchii had the most stable bacterial community under heat stress (Camp et al., 2020). Additionally, environmental adaptation of corals probably involves multiple members of the meta‐organism (e.g., coral, bacteria, Symbiodiniaceae; van Oppen et al., 2018).…”