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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.

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Variability of holobiont respiration rate, animal host- and algal symbiont citrate synthase (CS) specific activities, host biomass, and symbiont density within a natural population of Exaiptasia pallida. (A,B,D) Linear regression analysis of algal symbiont density (cells mg−1) as a predictor of (A) holobiont respiration rate normalized to host protein content (μmol O2mg−1 h−1), (B) host CS specific activity (U mg−1), and (D) symbiont CS specific activity (U mg−1). (C) Linear regression analysis of natural-log-transformed host biomass (mg protein) as a predictor of natural-log-transformed host CS specific activity (U mg−1). Relationships in (A–C) are statistically significant at p < 0.001 (D, p > 0.05). See text for details of multiple regression analysis of the data in (B,C).
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Figure 3: Variability of holobiont respiration rate, animal host- and algal symbiont citrate synthase (CS) specific activities, host biomass, and symbiont density within a natural population of Exaiptasia pallida. (A,B,D) Linear regression analysis of algal symbiont density (cells mg−1) as a predictor of (A) holobiont respiration rate normalized to host protein content (μmol O2mg−1 h−1), (B) host CS specific activity (U mg−1), and (D) symbiont CS specific activity (U mg−1). (C) Linear regression analysis of natural-log-transformed host biomass (mg protein) as a predictor of natural-log-transformed host CS specific activity (U mg−1). Relationships in (A–C) are statistically significant at p < 0.001 (D, p > 0.05). See text for details of multiple regression analysis of the data in (B,C).

Mentions: In naturally symbiotic E. pallida, holobiont respiration rate (mg host protein−1) and host CS specific activity were both positively associated with algal symbiont density (Figures 3A,B, Table 3). However, we also observed a negative log-linear relationship between host specific CS activity and anemone biomass (total animal DNA content; Figure 3C). Therefore, a multiple regression model was applied in order to parse the effects of these two covariates. Symbiont density alone explained 55.4% of variance in natural log-transformed host CS activity (see Table 3 for regression analysis parameters). Including total animal DNA (natural log-transformed) as a predictor increased the explained variance to 73.6% [tbiomass = −5.653, p < 0.0001; Full model: F(2, 46) = 67.79, p < 0.0001]. Alone, total animal DNA explained 38.5% of variation in host specific CS activity [tbiomass = −5.574, p < 0.0001; Full model: F(1, 47) = 31.07, p < 0.0001]. A weak negative association (statistically significant only for the y-intercept) was noted between symbiont CS specific activity and algal symbiont density (Figure 3D, Table 3).


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)

Variability of holobiont respiration rate, animal host- and algal symbiont citrate synthase (CS) specific activities, host biomass, and symbiont density within a natural population of Exaiptasia pallida. (A,B,D) Linear regression analysis of algal symbiont density (cells mg−1) as a predictor of (A) holobiont respiration rate normalized to host protein content (μmol O2mg−1 h−1), (B) host CS specific activity (U mg−1), and (D) symbiont CS specific activity (U mg−1). (C) Linear regression analysis of natural-log-transformed host biomass (mg protein) as a predictor of natural-log-transformed host CS specific activity (U mg−1). Relationships in (A–C) are statistically significant at p < 0.001 (D, p > 0.05). See text for details of multiple regression analysis of the data in (B,C).
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Related In: Results  -  Collection

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Figure 3: Variability of holobiont respiration rate, animal host- and algal symbiont citrate synthase (CS) specific activities, host biomass, and symbiont density within a natural population of Exaiptasia pallida. (A,B,D) Linear regression analysis of algal symbiont density (cells mg−1) as a predictor of (A) holobiont respiration rate normalized to host protein content (μmol O2mg−1 h−1), (B) host CS specific activity (U mg−1), and (D) symbiont CS specific activity (U mg−1). (C) Linear regression analysis of natural-log-transformed host biomass (mg protein) as a predictor of natural-log-transformed host CS specific activity (U mg−1). Relationships in (A–C) are statistically significant at p < 0.001 (D, p > 0.05). See text for details of multiple regression analysis of the data in (B,C).
Mentions: In naturally symbiotic E. pallida, holobiont respiration rate (mg host protein−1) and host CS specific activity were both positively associated with algal symbiont density (Figures 3A,B, Table 3). However, we also observed a negative log-linear relationship between host specific CS activity and anemone biomass (total animal DNA content; Figure 3C). Therefore, a multiple regression model was applied in order to parse the effects of these two covariates. Symbiont density alone explained 55.4% of variance in natural log-transformed host CS activity (see Table 3 for regression analysis parameters). Including total animal DNA (natural log-transformed) as a predictor increased the explained variance to 73.6% [tbiomass = −5.653, p < 0.0001; Full model: F(2, 46) = 67.79, p < 0.0001]. Alone, total animal DNA explained 38.5% of variation in host specific CS activity [tbiomass = −5.574, p < 0.0001; Full model: F(1, 47) = 31.07, p < 0.0001]. A weak negative association (statistically significant only for the y-intercept) was noted between symbiont CS specific activity and algal symbiont density (Figure 3D, Table 3).

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