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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.


Relationship between the proportion of total holobiont citrate synthase (CS) activity that is symbiont-derived (RSym) and the contribution of symbiont biomass (measured as protein) to the total holobiont biomass (1-ß, see Muscatine et al., 1981) in (A) a natural population of Exaiptasia pallida and (B) two groups of E. pallida re-infected with either Symbiodinium type A4 or Symbiodinium minutum. The dotted line in (A) describes y = x. The solid lines describe the actual relationship between RSym and 1-ß in each group of animals, and are statistically significant at p < 0.001.
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Figure 4: Relationship between the proportion of total holobiont citrate synthase (CS) activity that is symbiont-derived (RSym) and the contribution of symbiont biomass (measured as protein) to the total holobiont biomass (1-ß, see Muscatine et al., 1981) in (A) a natural population of Exaiptasia pallida and (B) two groups of E. pallida re-infected with either Symbiodinium type A4 or Symbiodinium minutum. The dotted line in (A) describes y = x. The solid lines describe the actual relationship between RSym and 1-ß in each group of animals, and are statistically significant at p < 0.001.

Mentions: Analysis of CS enzyme activity as an indicator of aerobic capacity allowed us to estimate the partitioning of respiratory activity between host and symbiont and relate this to symbiont biomass. The symbiont biomass fraction (1-ß; as defined by Muscatine et al., 1981) ranged from 0.03 to 0.21 in our natural E. pallida population, with a median value of 0.09 (n = 53). These data are plotted against the symbiont-respiration fraction (RSym) in Figure 4A, alongside a line with slope = 1 describing equality between 1-ß and RSym. Concretely, any point above (or below) this line represents a holobiont with a higher (or lower) RSym than would be expected from the value of 1-ß. The slope of the fitted regression line was significantly different from unity [F(1, 49) = 38.03, p < 0.0001; Slope = 0.689[(95 %CI:0.475, 0.900), t = 6.167, p < 0.0001]], which suggests that RSym and 1-ß are not equivalent in our naturally symbiotic E. pallida anemones.


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)

Relationship between the proportion of total holobiont citrate synthase (CS) activity that is symbiont-derived (RSym) and the contribution of symbiont biomass (measured as protein) to the total holobiont biomass (1-ß, see Muscatine et al., 1981) in (A) a natural population of Exaiptasia pallida and (B) two groups of E. pallida re-infected with either Symbiodinium type A4 or Symbiodinium minutum. The dotted line in (A) describes y = x. The solid lines describe the actual relationship between RSym and 1-ß in each group of animals, and are statistically significant at p < 0.001.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 4: Relationship between the proportion of total holobiont citrate synthase (CS) activity that is symbiont-derived (RSym) and the contribution of symbiont biomass (measured as protein) to the total holobiont biomass (1-ß, see Muscatine et al., 1981) in (A) a natural population of Exaiptasia pallida and (B) two groups of E. pallida re-infected with either Symbiodinium type A4 or Symbiodinium minutum. The dotted line in (A) describes y = x. The solid lines describe the actual relationship between RSym and 1-ß in each group of animals, and are statistically significant at p < 0.001.
Mentions: Analysis of CS enzyme activity as an indicator of aerobic capacity allowed us to estimate the partitioning of respiratory activity between host and symbiont and relate this to symbiont biomass. The symbiont biomass fraction (1-ß; as defined by Muscatine et al., 1981) ranged from 0.03 to 0.21 in our natural E. pallida population, with a median value of 0.09 (n = 53). These data are plotted against the symbiont-respiration fraction (RSym) in Figure 4A, alongside a line with slope = 1 describing equality between 1-ß and RSym. Concretely, any point above (or below) this line represents a holobiont with a higher (or lower) RSym than would be expected from the value of 1-ß. The slope of the fitted regression line was significantly different from unity [F(1, 49) = 38.03, p < 0.0001; Slope = 0.689[(95 %CI:0.475, 0.900), t = 6.167, p < 0.0001]], which suggests that RSym and 1-ß are not equivalent in our naturally symbiotic E. pallida anemones.

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.