Partner Switching and Metabolic Carbon Flux under Thermal Stress in the Cnidarian-Dinoflagellate Symbiosis DOI Creative Commons

Evan M. Heit

Published: Sept. 18, 2023

<p><strong>Reef corals depend heavily on their symbiotic relationship with dinoflagellates of the family Symbiodiniaceae, which are primary source metabolic energy and hence allow them to survive in oligotrophic tropical seas. The between these two partners is exceptionally sensitive environmental change, however, global warming known induce dysbiosis (i.e., breakdown symbiosis) a process referred as ‘coral bleaching’. adaptive bleaching hypothesis posits that host may acquire new dominant Symbiodiniaceae species after event, either from shift relative abundance resident symbionts (‘shuffling’) or uptake environment (‘switching’), better equipping holobiont whole for regime. However, different symbiont types have nutritional implications coral, potentially limiting potential partner shuffling switching. Energy-rich carbon compounds primarily provided by coral glucose, glycerol, lipids. Yet, it poorly understood how climate change impacts this translocation identity influences response. This thesis, therefore, addressed topic, using sea anemone Exaiptasia diaphana (‘Aiptasia’), globally adopted model system study cnidarian-dinoflagellate symbiosis.</strong></p><p>First, I aimed quantify compare pools carbon-based metabolites under thermal stress symbiont, focusing total carbohydrates (Chapter 2). It was hypothesized (33 °C) would cause decline various metabolites, likely due decreased photosynthetic function host, combined elevated catabolism stress. Metabolites were measured range commercially available metabolite-specific assay kits. As predicted, at high temperature, glucose glycerol remained constant even increased controls. latter observation consistent gluconeogenesis synthesis likes glycerol) response demands temperatures. other hand, use metabolite an osmolyte moderator cellular While test-kit approach used here associated considerable amount inter-sample variability, nevertheless confirmed added previous observations gained much more expensive, technically complex metabolomics methods.</p><p>I then compared photosynthates Aiptasia low, control, temperature (15, 25, 33 oC), when colonized Breviolum minutum, only through Indo-Pacific region (the here), Durusdinium trenchii psygmophilum 3). D. thermally tolerant but opportunistic not typically Aiptasia, while often temperate sub-tropical species, including western Atlantic Ocean. B. minutum translocate photosynthate its control out-perform low temperatures, respectively. To test this, radiotracer (NaH14CO3) measure fixation translocation. Contrary expectations, anemones hosting bleached completely both population density controls, containing did bleach extensively those confirming reputation former ‘thermal generalist.’ With respect metabolism, performed similarly slightly out-performed across all though most benefit temperature. had major influence flux lessening impact bleaching. Specifically, facilitated proportionally higher rates symbiont-cell specific photosynthesis translocation, presumably reduced competition CO2, such heat-stressed continued receive similar amounts controls.</p><p>In summary, thesis demonstrates type metabolism symbiosis. Most interestingly, my findings highlight importance research processes underlie physiology generalists aid adaptation reef natural development tools conservation.</p>

Language: Английский

Functional potential and evolutionary response to long-term heat selection of bacterial associates of coral photosymbionts DOI Creative Commons
Justin Maire, Gayle K. Philip, Jadzia Livingston

et al.

mSystems, Journal Year: 2023, Volume and Issue: 8(6)

Published: Nov. 1, 2023

Symbiotic microorganisms are crucial for the survival of corals and their resistance to coral bleaching in face climate change. However, impact microbe-microbe interactions on functioning is mostly unknown but could be essential factors adaption future climates. Here, we investigated between cultured dinoflagellates Symbiodiniaceae family, photosymbionts corals, associated bacteria. By assessing genomic potential 49 bacteria, found that they likely beneficial Symbiodiniaceae, through production B vitamins antioxidants. Additionally, bacterial genes involved host-symbiont interactions, such as secretion systems, accumulated mutations following long-term exposure heat, suggesting symbiotic may change under This highlights importance functioning.

Language: Английский

Citations

8
A novel, tissue-associated and vertically transmitted bacterial symbiont in the coralPocillopora acuta DOI Creative Commons
Justin Maire, Sarah Jane Tsang Min Ching, Katarina Damjanovic

et al.

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2023, Volume and Issue: unknown

Published: Sept. 14, 2023

Abstract Coral microhabitats are colonized by a myriad of microorganisms, including diverse bacteria which essential for host functioning and survival. However, the location, transmission, functions individual bacterial species living inside coral tissues remain poorly studied. Here, we show that previously undescribed symbiont Pocillopora acuta forms cell-associated microbial aggregates (CAMAs) within mesenterial filaments. CAMAs were found in both adults larval offspring, providing evidence vertical transmission. In situ laser capture microdissection followed 16S rRNA gene metabarcoding shotgun metagenomics produced near complete metagenome-assembled genome. We subsequently cultured CAMA from P. colonies, sequenced assembled their genomes. Phylogenetic analyses showed belong to an Endozoicomonadaceae genus species, propose name Sororendozoicomonas aggregata gen. nov sp. nov. Metabolic pathway reconstruction its genome sequence suggests this can synthesize most amino acids, several B vitamins, antioxidants, may be beneficial hosts. This study provides detailed insights into new member widespread family, thereby improving our understanding holobiont functioning. Vertically transmitted, tissue-associated bacteria, such as S. key candidates development microbiome manipulation approaches with long-term positive effects on host.

Language: Английский

Citations

1
Bleached coral supports high diversity and heterogeneity of bacterial communities: Following the rule of the ‘Anna Karenina principle’ DOI

Yihan Wei,

Wenguang Zhang,

Elnalee Buyagao Baguya

et al.

Environmental Research, Journal Year: 2024, Volume and Issue: 262, P. 119977 - 119977

Published: Sept. 13, 2024

Language: Английский

Citations

0
Functional potential and evolutionary response to long-term heat selection of bacterial associates of coral photosymbionts DOI Creative Commons
Justin Maire, Gayle K. Philip, Jadzia Livingston

et al.

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2023, Volume and Issue: unknown

Published: Aug. 4, 2023

Abstract Corals rely on a wide range of microorganisms for their functioning, including intracellular dinoflagellates (Symbiodiniaceae) and bacteria. Marine heatwaves trigger the loss Symbiodiniaceae from coral tissues - bleaching often leading to death. While coral-bacteria interactions are widely studied, Symbiodiniaceae-bacteria have remained largely uninvestigated. Here, we provide genomic analysis 49 bacteria, spanning 16 genera, that closely associate with six cultured species. We analyzed bacterial functional potential by focusing potentially beneficial functions host, B vitamin synthesis antioxidant abilities, which may be crucial heat tolerance in turn resistance thermal bleaching. These analyses suggest scavenging reactive oxygen species (through production carotenoids or enzymes), possibly transfer organic carbon host cells. Single nucleotide polymorphism between bacteria isolated wild-type heat-evolved cultures revealed exposure long-term elevated temperature has resulted mutations genes known involved host-symbiont interactions, such as secretion systems. Climate change therefore modify how interact. This study provides an overview possible roles Symbiodiniaceae-associated functioning tolerance, reinforcing need further studies fully understand biology climate resilience. Importance Symbiotic survival corals face change. However, impact microbe-microbe is mostly unknown, but could essential factors adaption future climates. investigated family, photosymbionts corals, associated By assessing found they likely Symbiodiniaceae, through vitamins antioxidants. Additionally, systems, accumulated following heat, suggesting symbiotic under highlights importance functioning.

Language: Английский

Citations

0
Partner Switching and Metabolic Carbon Flux under Thermal Stress in the Cnidarian-Dinoflagellate Symbiosis DOI Creative Commons

Evan M. Heit

Published: Sept. 18, 2023

<p><strong>Reef corals depend heavily on their symbiotic relationship with dinoflagellates of the family Symbiodiniaceae, which are primary source metabolic energy and hence allow them to survive in oligotrophic tropical seas. The between these two partners is exceptionally sensitive environmental change, however, global warming known induce dysbiosis (i.e., breakdown symbiosis) a process referred as ‘coral bleaching’. adaptive bleaching hypothesis posits that host may acquire new dominant Symbiodiniaceae species after event, either from shift relative abundance resident symbionts (‘shuffling’) or uptake environment (‘switching’), better equipping holobiont whole for regime. However, different symbiont types have nutritional implications coral, potentially limiting potential partner shuffling switching. Energy-rich carbon compounds primarily provided by coral glucose, glycerol, lipids. Yet, it poorly understood how climate change impacts this translocation identity influences response. This thesis, therefore, addressed topic, using sea anemone Exaiptasia diaphana (‘Aiptasia’), globally adopted model system study cnidarian-dinoflagellate symbiosis.</strong></p><p>First, I aimed quantify compare pools carbon-based metabolites under thermal stress symbiont, focusing total carbohydrates (Chapter 2). It was hypothesized (33 °C) would cause decline various metabolites, likely due decreased photosynthetic function host, combined elevated catabolism stress. Metabolites were measured range commercially available metabolite-specific assay kits. As predicted, at high temperature, glucose glycerol remained constant even increased controls. latter observation consistent gluconeogenesis synthesis likes glycerol) response demands temperatures. other hand, use metabolite an osmolyte moderator cellular While test-kit approach used here associated considerable amount inter-sample variability, nevertheless confirmed added previous observations gained much more expensive, technically complex metabolomics methods.</p><p>I then compared photosynthates Aiptasia low, control, temperature (15, 25, 33 oC), when colonized Breviolum minutum, only through Indo-Pacific region (the here), Durusdinium trenchii psygmophilum 3). D. thermally tolerant but opportunistic not typically Aiptasia, while often temperate sub-tropical species, including western Atlantic Ocean. B. minutum translocate photosynthate its control out-perform low temperatures, respectively. To test this, radiotracer (NaH14CO3) measure fixation translocation. Contrary expectations, anemones hosting bleached completely both population density controls, containing did bleach extensively those confirming reputation former ‘thermal generalist.’ With respect metabolism, performed similarly slightly out-performed across all though most benefit temperature. had major influence flux lessening impact bleaching. Specifically, facilitated proportionally higher rates symbiont-cell specific photosynthesis translocation, presumably reduced competition CO2, such heat-stressed continued receive similar amounts controls.</p><p>In summary, thesis demonstrates type metabolism symbiosis. Most interestingly, my findings highlight importance research processes underlie physiology generalists aid adaptation reef natural development tools conservation.</p>

Language: Английский

Citations

0