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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.


Scatterplots of the relationships in Exaiptasia pallida between mitochondrial genome copy number (mtDNA/nucDNA ratio) and (A) holobiont respiration rate normalized to host protein content (μmol O2mg−1 h−1) and (B) host citrate synthase (CS) specific activity (U mg−1). Closed symbols represent values obtained using the mitochondrial cytochrome c oxidase subunit 1 (CO1) gene, while open symbols represent values obtained using the mitochondrial ATP-synthase subunit 6 (ATP6) gene. Copy numbers for both genes were normalized to that of eukaryotic translation elongation factor 1 alpha (EF-1-α), a single-copy nuclear gene in E. pallida. Neither of the relationships in (A,B) was statistically significant at p < 0.05. (C) Strong positive association between mtDNA/nucDNA as calculated using CO1 and ATP6 copy numbers normalized to EF-1-α.
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Figure 2: Scatterplots of the relationships in Exaiptasia pallida between mitochondrial genome copy number (mtDNA/nucDNA ratio) and (A) holobiont respiration rate normalized to host protein content (μmol O2mg−1 h−1) and (B) host citrate synthase (CS) specific activity (U mg−1). Closed symbols represent values obtained using the mitochondrial cytochrome c oxidase subunit 1 (CO1) gene, while open symbols represent values obtained using the mitochondrial ATP-synthase subunit 6 (ATP6) gene. Copy numbers for both genes were normalized to that of eukaryotic translation elongation factor 1 alpha (EF-1-α), a single-copy nuclear gene in E. pallida. Neither of the relationships in (A,B) was statistically significant at p < 0.05. (C) Strong positive association between mtDNA/nucDNA as calculated using CO1 and ATP6 copy numbers normalized to EF-1-α.

Mentions: In addition to analysis of CS activity, we tested whether the animal mitochondrial/nuclear genome ratio might be a useful indicator of mitochondrial density in E. pallida. The DNA extraction method had no effect on the mtDNA/nucDNA ratio (ESM Figure S2C). Therefore, data were pooled for subsequent analyses. Anemone mtDNA/nucDNA was highly variable (range = 20–300) and was not a significant predictor either of protein-normalized whole-organism respiration rate or anemone specific CS activity (Figures 2A,B). The very strong correlation between CO1/EF-1-a and ATP6/EF-1-a ratios (R2 > 0.95; Figure 2C) meant that this was the case regardless of which mitochondrial gene was used as the mtDNA target.


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)

Scatterplots of the relationships in Exaiptasia pallida between mitochondrial genome copy number (mtDNA/nucDNA ratio) and (A) holobiont respiration rate normalized to host protein content (μmol O2mg−1 h−1) and (B) host citrate synthase (CS) specific activity (U mg−1). Closed symbols represent values obtained using the mitochondrial cytochrome c oxidase subunit 1 (CO1) gene, while open symbols represent values obtained using the mitochondrial ATP-synthase subunit 6 (ATP6) gene. Copy numbers for both genes were normalized to that of eukaryotic translation elongation factor 1 alpha (EF-1-α), a single-copy nuclear gene in E. pallida. Neither of the relationships in (A,B) was statistically significant at p < 0.05. (C) Strong positive association between mtDNA/nucDNA as calculated using CO1 and ATP6 copy numbers normalized to EF-1-α.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 2: Scatterplots of the relationships in Exaiptasia pallida between mitochondrial genome copy number (mtDNA/nucDNA ratio) and (A) holobiont respiration rate normalized to host protein content (μmol O2mg−1 h−1) and (B) host citrate synthase (CS) specific activity (U mg−1). Closed symbols represent values obtained using the mitochondrial cytochrome c oxidase subunit 1 (CO1) gene, while open symbols represent values obtained using the mitochondrial ATP-synthase subunit 6 (ATP6) gene. Copy numbers for both genes were normalized to that of eukaryotic translation elongation factor 1 alpha (EF-1-α), a single-copy nuclear gene in E. pallida. Neither of the relationships in (A,B) was statistically significant at p < 0.05. (C) Strong positive association between mtDNA/nucDNA as calculated using CO1 and ATP6 copy numbers normalized to EF-1-α.
Mentions: In addition to analysis of CS activity, we tested whether the animal mitochondrial/nuclear genome ratio might be a useful indicator of mitochondrial density in E. pallida. The DNA extraction method had no effect on the mtDNA/nucDNA ratio (ESM Figure S2C). Therefore, data were pooled for subsequent analyses. Anemone mtDNA/nucDNA was highly variable (range = 20–300) and was not a significant predictor either of protein-normalized whole-organism respiration rate or anemone specific CS activity (Figures 2A,B). The very strong correlation between CO1/EF-1-a and ATP6/EF-1-a ratios (R2 > 0.95; Figure 2C) meant that this was the case regardless of which mitochondrial gene was used as the mtDNA target.

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.