Heterotrophic Carbon Fixation in a Salamander-Alga Symbiosis

Abstract

The unique symbiosis between a vertebrate salamander, Ambystoma maculatum, and unicellular green alga, Oophila amblystomatis, involves multiple modes of interaction. These include an ectosymbiotic interaction where the alga colonizes the egg capsule, and an intracellular interaction where the alga enters tissues and cells of the salamander. One common interaction in mutualist photosymbioses is the transfer of photosynthate from the algal symbiont to the host animal. In the A. maculatum-O. amblystomatis interaction, there is conflicting evidence regarding whether the algae in the egg capsule transfer chemical energy captured during photosynthesis to the developing salamander embryo. In experiments where we took care to separate the carbon fixation contributions of the salamander embryo and algal symbionts, we show that inorganic carbon fixed by A. maculatum embryos reaches 2% of the inorganic carbon fixed by O. amblystomatis algae within an egg capsule after 2 h in the light. After 2 h in the dark, inorganic carbon fixed by A. maculatum embryos is 800% of the carbon fixed by O. amblystomatis algae within an egg capsule. Using photosynthesis inhibitors, we show that A. maculatum embryos and O. amblystomatis algae compete for available inorganic carbon within the egg capsule environment. Our results confirm earlier studies suggesting a role of heterotrophic carbon fixation during vertebrate embryonic development. Our results also show that the considerable capacity of developing A. maculatum embryos for inorganic carbon fixation precludes our ability to distinguish any minor role of photosynthetically transferred carbon from algal symbionts to host salamanders using bicarbonate introduced to the egg system as a marker.

Toward Photosynthetic Mammalian Cells through Artificial Endosymbiosis

“…Until now, the majority of documented natural endosymbiotic relationships have been observed in invertebrates. [ 29 ] However, establishing long‐term symbiotic relationships between microorganisms and mammalian cells has proven challenging due to the high degree of evolution and exclusivity characterizing mammalian cells. While mammalian macrophages are capable of spontaneously phagocytosing cyanobacteria, it has been demonstrated that they are ill‐suited to function as host cells for endosymbiosis with cyanobacteria, primarily due to their robust immune responses.…”

Green oxygen power plants in the brain rescue neuronal activity

“…Moreover, injection of these green algae into zebrafish eggs formed chimeras that remained viable for several days and after subsequent extraction from the larvae, the algae continued to grow (Alvarez et al, 2015). This suggests that the period of amalgamation with an animal had no obvious detrimental impact on the fertility of these phototrophic microorganisms in line with natural symbiotic interactions between algae and vertebrates (Burns et al, 2020;Kerney et al, 2011). Moreover, the employment of Xenopus tadpoles at mid-larval stages for experiments such as presented here might be advantageous for further exploring the beneficial range of systemically introduced phototrophic microorganisms on brain metabolism and electrical activity because the innate immune system in these animals is only completed after metamorphosis (Godwin and Rosenthal, 2014).…”

“…Provided photosynthetic microorganisms such as algae and cyanobacteria can be inserted and distributed throughout the tissue such as the brain, their O 2 -producing ability might directly supplement the respective needs of animals. In fact, natural symbiotic interactions between such microorganisms and animals are reported for members of the phyla Porifera (sponges), Cnidaria (corals, sea anemones; Venn et al., 2008 ) and also salamander species ( Burns et al., 2020 ; Kerney et al., 2011 ). By mimicking this natural principle, microalgae have occasionally been employed in biomedical science as efficient O 2 source, mostly to supplant absent blood perfusion of isolated tissue ( Chávez et al., 2020 ).…”

Diversity and substrate-specificity of green algae and other micro-eukaryotes colonizing amphibian clutches in Germany, revealed by DNA metabarcoding

“…Oophila within the capsular chamber provide an increase in the partial pressure of oxygen during the day, potentially remove nitrogenous waste, and have been reported to transfer photosynthate to the amphibian embryos (Bachmann et al 1986 ; Goff and Stein 1978 ; Graham et al 2013 ; Kerney 2011 ; Pinder and Friet 1994 ), which may lead to acceleration of embryonal development, larger sized embryos, increased viability and hatching success (Gilbert 1942 , 1944 ). However, other studies have reported no measurable exchange of photosynthate from algae to amphibian embryos (Burns et al 2020 ). Additional effects by the algae, such as a reduction of micro-organisms that are potentially harmful to the host, have been hypothesized (Kim et al 2014 ) but not yet tested.…”

“…gracile (Kerney et al 2019 ; Marco and Blaustein 2000 ) egg capsule chambers. These O. amblystomatis isolates have been used in studies of gene expression (Burns et al 2017 ; Kerney et al 2019 ), carbon fixation (Burns et al 2020 ), and host-symbiont fidelity (Kerney et al 2019 ). As an exception, a few isolates from A .…”