Endosymbiosis: Gasping for air
Transcriptomics is shedding new light on the relationship between photosynthetic algae and salamander eggs.
- UMR8576 University of Lille/CNRS, France
Primary endosymbiosis involves the penetration of single cell bacteria into the cytoplasm of eukaryotic host cells, whereas secondary endosymbiosis involves single cell eukaryotes entering eukaryotic host cells. Both of these forms of endosymbiosis are usually followed by many different types of symbiotic interactions. Moreover, certain organelles found in eukaryotic cells, notably mitochondria and plastids, are the result of endosymbiosis.
Endosymbiosis is rather rare in vertebrates, mainly because their immune system is likely to fend off any invaders. So what challenges do potential symbionts face upon entering a potentially hostile intracellular environment? Now, in eLife, John Burns of the American Museum of Natural History, Ryan Kerney of Gettysburg College and colleagues provide a surprising answer to these questions (Burns et al., 2017).
A well-known example of a symbiotic relationship is that of the green Volvocean alga Oophila amblystomatis, and the spotted salamander Ambystoma maculatum. These algae are photosynthetic, so they use light energy to produce sugar and oxygen. Oophila algae also need oxygen to survive, but they can withstand anoxia (that is, a total lack of oxygen) for short periods of time.
It has been shown that Oophila algae grow better in water populated with salamander embryos, and the salamander embryos are healthier when more algae are present. Initially, it was thought that the alga and the salamander form an ectosymbiotic relationship, where the alga grows around the eggs of the salamander and supplies the embryo with oxygen and sugar in exchange for waste products (Graham et al., 2013; Small et al., 2014). However, it was recently discovered that these ectosymbionts can reach and penetrate into embryo cells to also form an endosymbiotic relationship, with the alga living inside the embryo cells of the salamander (Kerney et al., 2011).
To better understand the molecular mechanisms underlying this relationship, Burns et al. used a technique called differential expression RNA-seq analysis to compare the transcriptomes (that is, all the gene transcripts) of three different types of algae: ectosymbiotic algae that lived around the egg; endosymbiotic algae that lived inside the embryos; and algae that were grown in the laboratory (Burns et al., 2017). In addition, they compared the transcriptomes of the salamander embryo cells that either contained or lacked the algae.
The technical originality and finesse of this approach lie in the comparison between ecto- and endosymbiotic transcriptomes of the algae: studying the different types of symbiotic relationships that occur within the same individual helps to provide a clearer picture of the molecular mechanisms that shape these processes.
Burns et al. discovered that the endosymbiotic algae experienced a shift from an oxidative metabolism to a fermentative metabolism. The algae also experienced a clear increase in transcripts from genes of algal fermentative metabolism, including an increase of hydrogenase, which is the hallmark of a switch to anoxia (Grossman et al., 2011). This was accompanied by a reduction in transcripts of core components of photosystem II (which produces oxygen) and mitochondrial complex I. This response mirrors the response of the related green alga Chlamydomonas reinhardti to an absence of sulfur, which involves a reduction in oxygen production by photosystem II, as well as reductions in sulfate transport and sulfur metabolism (Nguyen et al., 2008).
The limitations imposed on photosynthesis by shortages of oxygen and/or sulfur, combined with a lack of light inside the embryonic cells, means that very little carbon fixation will occur. This is consistent with previous work which showed that immotile endosymbionts display lower levels of starch than free-swimming ectosymbionts, despite the fact that swimming has been demonstrated to have a strong negative impact on starch accumulation in C. reinhardti (Hamilton et al., 1992).
In addition to those symptoms related to a lack of oxygen, the algae inside the embryo showed signs of cellular stress and had higher levels of proteins that are usually expressed in response to stressors such as heat shock or autophagy. Hence, the endosymbionts are likely gasping for air and actively breaking down their polysaccharide stores by fermentation, which is a well-known response to hypoxia in Volvocean algae (Klein and Betz, 1978). Given these circumstances, it seems rather unlikely that the endosymbiotic algae are in a position to supply significant amounts of either oxygen or photosynthate to the embryo cells. It remains thus unclear how these cells may actually benefit from the presence of the algae.
The dramatic response of the endosymbiotic algae to a lack of oxygen somewhat resembles the responses that occur in certain intracellular parasites (Polonais and Soldati-Favre, 2010) or bacteria. These microorganisms show similar stress responses and need fermentation to create energy. In addition, some bacteria use a specific enzyme with a high affinity to oxygen to initiate a cellular ‘microaerophilic’ response when oxygen is scarce or unavailable (Juul et al., 2007; Omsland et al., 2013).
The embryo cells, on the other hand, appeared to be rather unfazed by the algae living inside them. Modifications in their gene transcripts suggested a lowered innate immune response, and while the embryo cells with endosymbiotic algae experienced changes in their metabolic signaling pathways, they did not exhibit any signs of stress.
The work by Burns et al. highlights the problems a lack of oxygen in the intracellular environment can pose for photosynthetic algae, once they have managed to breach the immune defenses of their host. The unexpected shortage of sulfur inside the host cell exacerbates these problems, leading to a switch to fermentative metabolism. It is thought that primary or secondary plastids – organelles found in plants and algae that are responsible for producing and storing food – evolved from comparable photosynthetic endosymbionts (cyanobacteria or eukaryotic algae) that had to address these and other challenges.
References
-
Intracapsular algae provide fixed carbon to developing embryos of the salamander Ambystoma maculatumJournal of Experimental Biology 216:452–459.https://doi.org/10.1242/jeb.076711
-
Accumulation of starch in Chlamydomonas reinhardtii flagellar mutantsBiochemistry and Cell Biology 70:255–258.https://doi.org/10.1139/o92-039
-
Characterization of in vitro chlamydial cultures in low-oxygen atmospheresJournal of Bacteriology 189:6723–6726.https://doi.org/10.1128/JB.00279-07
-
Fermentative metabolism of hydrogen-evolving Chlamydomonas moewusiiPlant Physiology 61:953–956.https://doi.org/10.1104/pp.61.6.953
-
Versatility in the acquisition of energy and carbon sources by the ApicomplexaBiology of the Cell 102:435–445.https://doi.org/10.1042/BC20100005
Article and author information
Author details
Publication history
- Version of Record published: May 2, 2017 (version 1)
Copyright
© 2017, Ball et al.
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 1,612
- views
-
- 155
- downloads
-
- 2
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Endosymbiosis: Gasping for air
eLife 6:e27004.
https://doi.org/10.7554/eLife.27004
Further reading
-
- Ecology
- Epidemiology and Global Health
Zoonotic disease dynamics in wildlife hosts are rarely quantified at macroecological scales due to the lack of systematic surveys. Non-human primates (NHPs) host Plasmodium knowlesi, a zoonotic malaria of public health concern and the main barrier to malaria elimination in Southeast Asia. Understanding of regional P. knowlesi infection dynamics in wildlife is limited. Here, we systematically assemble reports of NHP P. knowlesi and investigate geographic determinants of prevalence in reservoir species. Meta-analysis of 6322 NHPs from 148 sites reveals that prevalence is heterogeneous across Southeast Asia, with low overall prevalence and high estimates for Malaysian Borneo. We find that regions exhibiting higher prevalence in NHPs overlap with human infection hotspots. In wildlife and humans, parasite transmission is linked to land conversion and fragmentation. By assembling remote sensing data and fitting statistical models to prevalence at multiple spatial scales, we identify novel relationships between P. knowlesi in NHPs and forest fragmentation. This suggests that higher prevalence may be contingent on habitat complexity, which would begin to explain observed geographic variation in parasite burden. These findings address critical gaps in understanding regional P. knowlesi epidemiology and indicate that prevalence in simian reservoirs may be a key spatial driver of human spillover risk.
-
- Computational and Systems Biology
- Ecology
Collaborative hunting, in which predators play different and complementary roles to capture prey, has been traditionally believed to be an advanced hunting strategy requiring large brains that involve high-level cognition. However, recent findings that collaborative hunting has also been documented in smaller-brained vertebrates have placed this previous belief under strain. Here, using computational multi-agent simulations based on deep reinforcement learning, we demonstrate that decisions underlying collaborative hunts do not necessarily rely on sophisticated cognitive processes. We found that apparently elaborate coordination can be achieved through a relatively simple decision process of mapping between states and actions related to distance-dependent internal representations formed by prior experience. Furthermore, we confirmed that this decision rule of predators is robust against unknown prey controlled by humans. Our computational ecological results emphasize that collaborative hunting can emerge in various intra- and inter-specific interactions in nature, and provide insights into the evolution of sociality.
