Transcriptome Reprogramming of Symbiodiniaceae Breviolum minutum in Response to Casein Amino Acids Supplementation

Abstract

Dinoflagellates in the family Symbiodiniaceae can live freely in ocean waters or form a symbiosis with a variety of cnidarians including corals, sea anemones, and jellyfish. Trophic plasticity of Symbiodiniaceae is critical to its ecological success as it moves between environments. However, the molecular mechanisms underlying these trophic shifts in Symbiodiniaceae are still largely unknown. Using Breviolum minutum strain SSB01 (designated SSB01) as a model, we showed that Symbiodiniaceae go through a physiological and transcriptome reprogramming when the alga is grown with the organic nitrogen containing nutrients in hydrolyzed casein, but not with inorganic nutrients. SSB01 grows at a much faster rate and maintains stable photosynthetic efficiency when supplemented with casein amino acids compared to only inorganic nutrients or seawater. These physiological changes are driven by massive transcriptome changes in SSB01 supplemented with casein amino acids. The levels of transcripts encoding proteins involved in altering DNA conformation such as DNA topoisomerases, histones, and chromosome structural components were all significantly changed. Functional enrichment analysis also revealed processes involved in translation, ion transport, generation of second messengers, and phosphorylation. The physiological and molecular changes that underlie in vitro trophic transitions in Symbiodiniaceae can serve as an orthogonal platform to further understand the factors that impact the Symbiodiniaceae lifestyle.

Antibiotics Alter Pocillopora Coral-Symbiodiniaceae-Bacteria Interactions and Cause Microbial Dysbiosis During Heat Stress

“…The role of amino acids in generating energy via the TCA cycle (Akram, 2014) or alternatively as metabolites in chlorophyll biosynthesis (Vavilin and Vermaas, 2002) could potentially play a role in Cladocopium photosynthetic impairment. This second hypothesis is consistent with observations of decreased chlorophyll a in nitrogen-starved C. goreauii (Zhou et al, 2021) and stable photochemical efficiency and dramatically increased growth rates in Breviolium minutum cultures supplemented with casein amino acids (Kirk et al, 2020). Although the Pocillopora and Cladocopium genomes possess pathways for synthesizing most amino acids and heterotrophic feeding may account for substantial input of essential amino acids to the coral holobiont (Fox et al, 2019;Ferrier-Pagès et al, 2021), these observations suggest that certain coral-associated and/or Symbiodiniaceae-associated bacteria may provide in hospite Symbiodiniaceae with additional nitrogenous compounds that benefit holobiont metabolism (Benavides et al, 2017;Geissler et al, 2021;Glaze et al, 2021;Rädecker et al, 2021).…”

Cnidarian-Symbiodiniaceae symbiosis establishment is independent of photosynthesis

“…Photosynthesis is not required for proliferation in some cnidarian-Symbiodiniaceae relationships Symbiodiniaceae have a flexible metabolism that allows them to grow and divide in a variety of environments. 24,55 Supplied only with inorganic nutrients and light, Symbiodiniaceae can grow autotrophically with photosynthesis. However, if given fixed carbon sources, they can grow heterotrophically.…”

Symbiodiniaceae Are the First Site of Heterotrophic Nitrogen Assimilation in Reef-Building Corals

“…Even in complete darkness for several weeks, symbionts continue to assimilate heterotrophically derived nitrogen. As recently shown with Breviolum minutum strain SSB01 maintained in culture, direct supplementation of Symbiodiniaceae with amino acids can allow them to grow at a much higher rate and to maintain a more stable photosynthetic efficiency compared to when they are supplied with inorganic nutrients or seawater ( 39 ).…”

“…In S. pistillata , the significant increase (imaged in red color) in TP Glx-Phe , δ 15 N-AAs and δ 13 C-AAs in symbionts and host tissue with plankton feeding compared to unfed conditions indicatesd that the amino acids (AAs) were incorporated directly in host and symbiont biomass. AAs were transferred from host to symbiont through amino acid transporters ( 1 , 2 , 39 , 40 ). In T. reniformis , the lack of change (imaged in black color) in TP Glx-Phe , and δ 13 C-AAs in symbionts with plankton feeding compared to unfed conditions indicated that the amino acids (AAs) were first recycled into ammonium (NH 4 ), before being transferred via transporters ( 3 , 4 , 39 , 40 ).…”

“…AAs were transferred from host to symbiont through amino acid transporters ( 1 , 2 , 39 , 40 ). In T. reniformis , the lack of change (imaged in black color) in TP Glx-Phe , and δ 13 C-AAs in symbionts with plankton feeding compared to unfed conditions indicated that the amino acids (AAs) were first recycled into ammonium (NH 4 ), before being transferred via transporters ( 3 , 4 , 39 , 40 ). to the symbionts and transformed into new AAs.…”