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Partitioning of Respiration in an Animal-Algal Symbiosis: Implications for Different Aerobic Capacity between Symbiodinium spp.

Hawkins TD, Hagemeyer JC, Hoadley KD, Marsh AG, Warner ME - Front Physiol (2016)

Bottom Line: In re-infected anemones, we found significant between-holobiont differences in the CS specific activity of the algal symbionts.Specifically, the long-held assumption of equivalency between symbiont/host biomass and respiration ratios can result in significant overestimation of symbiont respiration and potentially erroneous conclusions regarding the percentage of carbon translocated to the host.The interspecific variability in symbiont aerobic capacity provides further evidence for distinct physiological differences that should be accounted for when studying diverse host-symbiont combinations.

View Article: PubMed Central - PubMed

Affiliation: College of Earth, Ocean and Environment, School of Marine Science and Policy, University of Delaware Lewes, DE, USA.

ABSTRACT
Cnidarian-dinoflagellate symbioses are ecologically important and the subject of much investigation. However, our understanding of critical aspects of symbiosis physiology, such as the partitioning of total respiration between the host and symbiont, remains incomplete. Specifically, we know little about how the relationship between host and symbiont respiration varies between different holobionts (host-symbiont combinations). We applied molecular and biochemical techniques to investigate aerobic respiratory capacity in naturally symbiotic Exaiptasia pallida sea anemones, alongside animals infected with either homologous ITS2-type A4 Symbiodinium or a heterologous isolate of Symbiodinium minutum (ITS2-type B1). In naturally symbiotic anemones, host, symbiont, and total holobiont mitochondrial citrate synthase (CS) enzyme activity, but not host mitochondrial copy number, were reliable predictors of holobiont respiration. There was a positive association between symbiont density and host CS specific activity (mg protein(-1)), and a negative correlation between host- and symbiont CS specific activities. Notably, partitioning of total CS activity between host and symbiont in this natural E. pallida population was significantly different to the host/symbiont biomass ratio. In re-infected anemones, we found significant between-holobiont differences in the CS specific activity of the algal symbionts. Furthermore, the relationship between the partitioning of total CS activity and the host/symbiont biomass ratio differed between holobionts. These data have broad implications for our understanding of cnidarian-algal symbiosis. Specifically, the long-held assumption of equivalency between symbiont/host biomass and respiration ratios can result in significant overestimation of symbiont respiration and potentially erroneous conclusions regarding the percentage of carbon translocated to the host. The interspecific variability in symbiont aerobic capacity provides further evidence for distinct physiological differences that should be accounted for when studying diverse host-symbiont combinations.

No MeSH data available.


Related in: MedlinePlus

Predictive and correlative associations between animal host- and algal symbiont citrate synthase (CS) activity and holobiont respiration rate in a natural population of Exaiptasia pallida. (A) Linear regression analysis of total host CS activity (U) as a predictor of holobiont respiration rate (μmol O2 h−1); (B) Linear regression analysis of total holobiont CS activity (host + symbiont; U) as a predictor of holobiont respiration rate (μmol O2 h−1); (C) Pearson's correlation analysis of the relationship between host- and symbiont specific CS activities (U mg−1). All relationships are statistically significant at p < 0.001.
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Figure 1: Predictive and correlative associations between animal host- and algal symbiont citrate synthase (CS) activity and holobiont respiration rate in a natural population of Exaiptasia pallida. (A) Linear regression analysis of total host CS activity (U) as a predictor of holobiont respiration rate (μmol O2 h−1); (B) Linear regression analysis of total holobiont CS activity (host + symbiont; U) as a predictor of holobiont respiration rate (μmol O2 h−1); (C) Pearson's correlation analysis of the relationship between host- and symbiont specific CS activities (U mg−1). All relationships are statistically significant at p < 0.001.

Mentions: Total anemone citrate synthase (CS) activity was a significant predictor of holobiont respiration rate, explaining 82% of observed variance (Figure 1A, Table 2). In-hospite Symbiodinium CS activity was also a significant predictor of holobiont respiration (Table 2), although it explained less variation than did host CS (R2 = 0.70 vs. R2 = 0.82). The explained variance in holobiont respiration increased to 88% when total host and symbiont CS activities were combined (Figure 1B, Table 2).


Partitioning of Respiration in an Animal-Algal Symbiosis: Implications for Different Aerobic Capacity between Symbiodinium spp.

Hawkins TD, Hagemeyer JC, Hoadley KD, Marsh AG, Warner ME - Front Physiol (2016)

Predictive and correlative associations between animal host- and algal symbiont citrate synthase (CS) activity and holobiont respiration rate in a natural population of Exaiptasia pallida. (A) Linear regression analysis of total host CS activity (U) as a predictor of holobiont respiration rate (μmol O2 h−1); (B) Linear regression analysis of total holobiont CS activity (host + symbiont; U) as a predictor of holobiont respiration rate (μmol O2 h−1); (C) Pearson's correlation analysis of the relationship between host- and symbiont specific CS activities (U mg−1). All relationships are statistically significant at p < 0.001.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4834350&req=5

Figure 1: Predictive and correlative associations between animal host- and algal symbiont citrate synthase (CS) activity and holobiont respiration rate in a natural population of Exaiptasia pallida. (A) Linear regression analysis of total host CS activity (U) as a predictor of holobiont respiration rate (μmol O2 h−1); (B) Linear regression analysis of total holobiont CS activity (host + symbiont; U) as a predictor of holobiont respiration rate (μmol O2 h−1); (C) Pearson's correlation analysis of the relationship between host- and symbiont specific CS activities (U mg−1). All relationships are statistically significant at p < 0.001.
Mentions: Total anemone citrate synthase (CS) activity was a significant predictor of holobiont respiration rate, explaining 82% of observed variance (Figure 1A, Table 2). In-hospite Symbiodinium CS activity was also a significant predictor of holobiont respiration (Table 2), although it explained less variation than did host CS (R2 = 0.70 vs. R2 = 0.82). The explained variance in holobiont respiration increased to 88% when total host and symbiont CS activities were combined (Figure 1B, Table 2).

Bottom Line: In re-infected anemones, we found significant between-holobiont differences in the CS specific activity of the algal symbionts.Specifically, the long-held assumption of equivalency between symbiont/host biomass and respiration ratios can result in significant overestimation of symbiont respiration and potentially erroneous conclusions regarding the percentage of carbon translocated to the host.The interspecific variability in symbiont aerobic capacity provides further evidence for distinct physiological differences that should be accounted for when studying diverse host-symbiont combinations.

View Article: PubMed Central - PubMed

Affiliation: College of Earth, Ocean and Environment, School of Marine Science and Policy, University of Delaware Lewes, DE, USA.

ABSTRACT
Cnidarian-dinoflagellate symbioses are ecologically important and the subject of much investigation. However, our understanding of critical aspects of symbiosis physiology, such as the partitioning of total respiration between the host and symbiont, remains incomplete. Specifically, we know little about how the relationship between host and symbiont respiration varies between different holobionts (host-symbiont combinations). We applied molecular and biochemical techniques to investigate aerobic respiratory capacity in naturally symbiotic Exaiptasia pallida sea anemones, alongside animals infected with either homologous ITS2-type A4 Symbiodinium or a heterologous isolate of Symbiodinium minutum (ITS2-type B1). In naturally symbiotic anemones, host, symbiont, and total holobiont mitochondrial citrate synthase (CS) enzyme activity, but not host mitochondrial copy number, were reliable predictors of holobiont respiration. There was a positive association between symbiont density and host CS specific activity (mg protein(-1)), and a negative correlation between host- and symbiont CS specific activities. Notably, partitioning of total CS activity between host and symbiont in this natural E. pallida population was significantly different to the host/symbiont biomass ratio. In re-infected anemones, we found significant between-holobiont differences in the CS specific activity of the algal symbionts. Furthermore, the relationship between the partitioning of total CS activity and the host/symbiont biomass ratio differed between holobionts. These data have broad implications for our understanding of cnidarian-algal symbiosis. Specifically, the long-held assumption of equivalency between symbiont/host biomass and respiration ratios can result in significant overestimation of symbiont respiration and potentially erroneous conclusions regarding the percentage of carbon translocated to the host. The interspecific variability in symbiont aerobic capacity provides further evidence for distinct physiological differences that should be accounted for when studying diverse host-symbiont combinations.

No MeSH data available.


Related in: MedlinePlus