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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.


Patterns of respiration and photosynthesis in two groups of Exaiptasia pallida experimentally re-infected with homologous Symbiodinium ITS2-type A4 or heterologous, ITS2-type B1 S. minutum, respectively. (A) Symbiont cell densities (106 cells mg−1); (B) Symbiont photosynthetic output (pmol O2 cell−1 h−1); (C) Holobiont respiration rate normalized to host protein content (μmol O2mg−1 h−1); (D) Host (white box, black markers) and symbiont (gray box, white markers) specific citrate synthase (CS) activities (mU mg−1); (E) The proportion of symbiont-derived CS activity relative to total holobiont CS activity (RSym); (F) The relationship between RSym and symbiont biomass as a fraction of total biomass (1-ß; Muscatine et al., 1981). Boxes represent means (thick black line) ± 1 standard error, whiskers represent 1 standard deviation. Between-group comparisons for data in (A–C,F), and host CS specific activity in (D), were conducted using t-tests. Between-group comparisons for symbiont CS specific activity (D) and RSym(E) were conducted using Wilcoxon Rank-Sum tests.
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Figure 5: Patterns of respiration and photosynthesis in two groups of Exaiptasia pallida experimentally re-infected with homologous Symbiodinium ITS2-type A4 or heterologous, ITS2-type B1 S. minutum, respectively. (A) Symbiont cell densities (106 cells mg−1); (B) Symbiont photosynthetic output (pmol O2 cell−1 h−1); (C) Holobiont respiration rate normalized to host protein content (μmol O2mg−1 h−1); (D) Host (white box, black markers) and symbiont (gray box, white markers) specific citrate synthase (CS) activities (mU mg−1); (E) The proportion of symbiont-derived CS activity relative to total holobiont CS activity (RSym); (F) The relationship between RSym and symbiont biomass as a fraction of total biomass (1-ß; Muscatine et al., 1981). Boxes represent means (thick black line) ± 1 standard error, whiskers represent 1 standard deviation. Between-group comparisons for data in (A–C,F), and host CS specific activity in (D), were conducted using t-tests. Between-group comparisons for symbiont CS specific activity (D) and RSym(E) were conducted using Wilcoxon Rank-Sum tests.

Mentions: In anemones separately re-infected with homologous and heterologous Symbiodinium species, we noted significant differences in symbiont density and holobiont respiration, both of which were higher in animals hosting the homologous Symbiodinium A4 (Figures 5A,B). S. minutum displayed a higher rate of photosynthetic activity per cell than did Symbiodinium A4 (Figure 5C), and this pattern was repeated in its CS specific activity, which was significantly elevated relative to that of Symbiodinium A4 (Figure 5D). Host CS specific activity did not differ between the two groups (Figure 5D), and no significant difference was observed in RSym (Figure 5E, Table 4), despite there being a trend for higher RSym in the E. pallida-S. minutum holobiont. There was, however, a significant negative correlation between host- and symbiont specific CS activities in this particular symbiosis (Pearson's correlation test: r = −0.708, t = −4.139, df = 17, p = 0.0006). Median values for 1-ß for anemones hosting Symbiodinium A4 and S. minutum were similar at 0.08–0.09 (ranges: 0.02–0.16 and 0.04–0.14, respectively). However, the relationship between 1-ß and RSym differed between holobionts, with the slope close to unity for E. pallida-S. minutum symbioses, but significantly lower for the E. pallida-Symbiodinium A4 holobiont [Figure 4B; Linear regression: F(3, 34) = 18.04, p < 0.001; t(1−β × holobiont) = 3.404, p = 0.002]. These differences were mirrored in the RSym/1-ß ratios of individual anemones, which were significantly higher in animals hosting S. minutum (Table 4, Figure 5F).


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)

Patterns of respiration and photosynthesis in two groups of Exaiptasia pallida experimentally re-infected with homologous Symbiodinium ITS2-type A4 or heterologous, ITS2-type B1 S. minutum, respectively. (A) Symbiont cell densities (106 cells mg−1); (B) Symbiont photosynthetic output (pmol O2 cell−1 h−1); (C) Holobiont respiration rate normalized to host protein content (μmol O2mg−1 h−1); (D) Host (white box, black markers) and symbiont (gray box, white markers) specific citrate synthase (CS) activities (mU mg−1); (E) The proportion of symbiont-derived CS activity relative to total holobiont CS activity (RSym); (F) The relationship between RSym and symbiont biomass as a fraction of total biomass (1-ß; Muscatine et al., 1981). Boxes represent means (thick black line) ± 1 standard error, whiskers represent 1 standard deviation. Between-group comparisons for data in (A–C,F), and host CS specific activity in (D), were conducted using t-tests. Between-group comparisons for symbiont CS specific activity (D) and RSym(E) were conducted using Wilcoxon Rank-Sum tests.
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Figure 5: Patterns of respiration and photosynthesis in two groups of Exaiptasia pallida experimentally re-infected with homologous Symbiodinium ITS2-type A4 or heterologous, ITS2-type B1 S. minutum, respectively. (A) Symbiont cell densities (106 cells mg−1); (B) Symbiont photosynthetic output (pmol O2 cell−1 h−1); (C) Holobiont respiration rate normalized to host protein content (μmol O2mg−1 h−1); (D) Host (white box, black markers) and symbiont (gray box, white markers) specific citrate synthase (CS) activities (mU mg−1); (E) The proportion of symbiont-derived CS activity relative to total holobiont CS activity (RSym); (F) The relationship between RSym and symbiont biomass as a fraction of total biomass (1-ß; Muscatine et al., 1981). Boxes represent means (thick black line) ± 1 standard error, whiskers represent 1 standard deviation. Between-group comparisons for data in (A–C,F), and host CS specific activity in (D), were conducted using t-tests. Between-group comparisons for symbiont CS specific activity (D) and RSym(E) were conducted using Wilcoxon Rank-Sum tests.
Mentions: In anemones separately re-infected with homologous and heterologous Symbiodinium species, we noted significant differences in symbiont density and holobiont respiration, both of which were higher in animals hosting the homologous Symbiodinium A4 (Figures 5A,B). S. minutum displayed a higher rate of photosynthetic activity per cell than did Symbiodinium A4 (Figure 5C), and this pattern was repeated in its CS specific activity, which was significantly elevated relative to that of Symbiodinium A4 (Figure 5D). Host CS specific activity did not differ between the two groups (Figure 5D), and no significant difference was observed in RSym (Figure 5E, Table 4), despite there being a trend for higher RSym in the E. pallida-S. minutum holobiont. There was, however, a significant negative correlation between host- and symbiont specific CS activities in this particular symbiosis (Pearson's correlation test: r = −0.708, t = −4.139, df = 17, p = 0.0006). Median values for 1-ß for anemones hosting Symbiodinium A4 and S. minutum were similar at 0.08–0.09 (ranges: 0.02–0.16 and 0.04–0.14, respectively). However, the relationship between 1-ß and RSym differed between holobionts, with the slope close to unity for E. pallida-S. minutum symbioses, but significantly lower for the E. pallida-Symbiodinium A4 holobiont [Figure 4B; Linear regression: F(3, 34) = 18.04, p < 0.001; t(1−β × holobiont) = 3.404, p = 0.002]. These differences were mirrored in the RSym/1-ß ratios of individual anemones, which were significantly higher in animals hosting S. minutum (Table 4, Figure 5F).

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.