Differential carbon utilization and asexual reproduction under elevated pCO₂ conditions in the model anemone, Exaiptasia pallida, hosting different symbionts

Abstract

Here we report the effects of elevated pCO2 on the model symbiotic anemone Exaiptasia pallida and how its association with three different strains of the endosymbiotic dinoflagellate Symbiodinium minutum (ITS2‐type B1) affects its response. Exposure to elevated pCO2 (70.9 Pa) for 28 d led to an increased effective quantum yield of PSII in actinic light within two of the alga‐anemone combinations. Autotrophic carbon fixation, along with the rate of carbon translocated to the animal, were significantly elevated with high pCO2. Elevated pCO2 exposure also coincided with significantly greater asexual budding rates in all tested anemones. Further, differences in photochemistry and carbon translocation rates suggest subtle differences in the response to pCO2 among the three strains of S. minutum and their host anemones. This illustrates the potential for physiological diversity at the subspecies level for this ecologically important dinoflagellate. Positive alterations in photosynthesis, carbon utilization, and fitness within this model symbiosis suggest a potential benefit from ocean acidification (OA) not yet observed within corals, which may enable these anthozoans to gain a greater ecological presence under future OA conditions.

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

“…However, if mitochondrial copy number ratio is heritable (Ding et al, 2015 ), this variability may reflect a high genetic diversity within our E. pallida population. Preliminary analysis of microsatellite loci as described by Hoadley et al ( 2015 ) suggested that at least 60% of our anemones were genetically distinct individuals (data not shown). Likewise, anemone size was also highly variable in our natural population (range 0.1–2.0 mg total soluble protein) and mtDNA/nucDNA can vary with age (Simonetti et al, 1992 ; Barazzoni et al, 2000 ).…”

“…Novel E. pallida-Symbiodinium associations were established by exposing aposymbiotic anemones to one of two different Symbiodinium species (~1000 cells mL −1 in 500 mL seawater) according to the methods of Hoadley et al ( 2015 ). One group ( n > 30 animals) was incubated with a homologous, monoclonal Symbiodinium culture established from Symbiodinium originally isolated from the same E. pallida population and maintained in semi-continuous growth in f/2-Si culture media (Guillard, 1973 ) for period of at least 1 year.…”

“…However, estimates of how much photosynthetically fixed carbon is provided to the host and, implicitly, how much is retained by the algal symbionts, have depended largely on the use of two methods. The first measures photosynthetic fixation of 14 C- or 13 C-bicarbonate and its subsequent translocation into host tissues (Trench, 1971 ; Hofmann and Kremer, 1981 ; Muscatine et al, 1984 ; Gattuso et al, 1993 ; Davy and Cook, 2001 ; Hughes et al, 2010 ; Tremblay et al, 2012 , 2014 ; Hoadley et al, 2015 ; Kopp et al, 2015 ). The second technique, known as the “growth rate method,” relies on measurements of light- and dark oxygen fluxes alongside estimations of in-hospite symbiont growth rates and carbon contents (usually inferred from mitotic indices and cell volumes, respectively) to estimate the contribution of zooxanthellae (= Symbiodinium ) to animal respiration (commonly abbreviated as CZAR) (Muscatine et al, 1981 , 1983 ; McCloskey and Muscatine, 1984 ).…”

Warm-preconditioning protects against acute heat-induced respiratory dysfunction and delays bleaching in a symbiotic sea anemone

“…The corresponding increase in Symbiodinium P gross was somewhat surprising, as it occurred while F v /F m dropped. This could reflect the release of remaining Symbiodinium cells from carbon limitation as in hospite symbionts declined (Hoadley et al, 2015). Equally, it might have resulted in part from positive effects of heating on the rate of Symbiodinium A4 Rubisco activity (Galmés et al, 2015).…”

Unlocking the black‐box of inorganic carbon‐uptake and utilization strategies among coral endosymbionts (Symbiodiniaceae)

“…Photosynthetic responses retrieved from fluorometricand O 2 -based measurements provide insight into Ci uptake efficiency (Brading et al 2011;Oakley et al 2014;Roberty et al 2014;Suggett et al 2015;Grégoire et al 2017), yet few direct Ci assimilation rates have been performed to date despite early foundational work on coral endosymbionts (Al-Moghrabi et al 1996;Goiran et al 1996;Allemand et al 1998). More recent studies on Ci assimilation have adopted diverse approaches using stable ( 13 C; Pernice et al 2014;Baker et al 2018;Krueger et al 2018;Radecker et al 2018) and radioisotope methods ( 14 C; Brading et al 2013;Hoadley et al 2015Hoadley et al , 2016. As such, methodological differences across studies such as variable incubation lengths (Halsey et al 2013;Hughes et al 2018b) limit any reconciliation across species and environmental treatments.…”