Sunday 3 December 2017

Sponge bacterial symbionts, and not their host, accumulate high levels of toxic trace elements

Arsenic (As) and barium (Ba) are present in various forms as trace elements in sea water; arsenic is highly toxic and its levels in food are regulated under EU law (Commission Regulation 2015/1006), while soluble forms of barium are toxic to plants, terrestrial invertebrates and mammals to varying degrees (Menzie et al., 2008). A recent study reported the highest concentrations of arsenic and barium ever found in organisms from relatively unpolluted environments, in a common sponge from the Red Sea, Theonella swinhoei (Mayzel, Aizenberg & Ilan, 2014). As the authors note, sponges filter very high volumes of sea water (15000-24000 L d-1 kg tissue-1), therefore they have the potential to bioaccumulate trace compounds. A subsequent study found that the sponge-associated bacteria are enriched for arsenic and barium compared to the sponge cells, and that a few bacterial symbiont isolates can tolerate and precipitate arsenic (Keren et al., 2015). This lead the same researchers to carry out a more detailed study investigating the dynamics of As and Ba accumulation by T. swinhoei symbiotic bacteria (Keren et al., 2017). Using a combination of microscopy (SEM and TEM) and analytical techniques (X-ray spectrometry, MS), the authors discovered that:
a)    One bacterial symbiont, the filamentous bacterium Entotheonella sp., is specifically responsible for bioaccumulating As and Ba (6.07 and 11.7% weight ratios, respectively).
b)    The compounds are sequestered into lipid membrane-bound intracellular vesicles, where they are found in mineral form.
These findings are significant from both an ecological and an ecotoxicological perspective. Firstly, the detoxifying activity of Entotheonella sp. is likely to be of great importance to the host, and serves an analogous function to that of detoxifying organs in higher eukaryotes. In this respect, it would be interesting to conduct a manipulative experiment by removing the detoxifying symbionts and exposing the sponges to varying levels of As and Ba. In fact, although these chemicals are toxic to a wide range of organisms, it should not be assumed that the sponge relies entirely on its symbionts to survive exposure to such compounds. This is especially relevant considering the relatively high concentrations of As and Ba reported by Keren et al., 2017 in sponge cell fractions, albeit significantly lower than those of Entotheonella sp. cell fractions. Secondly, the fact that the mentioned symbiotic bacteria are able to mineralise As and Ba (thus rendering them insoluble) is of great promise for bioremediation: in fact, as with many other chemicals, their toxicity depends on their solubility (Menzie et al., 2008).
The study ultimately demonstrates the role of a specific sponge symbiont in sequestering the toxic trace elements As and Ba. Future studies should include manipulative experiments (cf above) in order to characterise the physiological implications of this phenomenon for the sponge holobiont.

Reviewed article:
Keren, R., Mayzel, B., Lavy, A., Polishchuk, I., Levy, D., Fakra, S. C., Pokroy, B. & Ilan, M. (2017) 'Sponge-associated bacteria mineralize arsenic and barium on intracellular vesicles'. Nature Communications, 8 pp. 14393.

References
Commission Regulation (EU) 2015/1006 of 25 June 2015 amending Regulation (EC) No 1881/2006 as regards maximum levels of inorganic arsenic in foodstuffs.

Keren, R., Lavy, A., Mayzel, B. & Ilan, M. (2015) 'Culturable associated-bacteria of the sponge Theonella swinhoei show tolerance to high arsenic concentrations'. Frontiers in Microbiology, 6 pp. 154.

Mayzel, B., Aizenberg, J. & Ilan, M. (2014) 'The Elemental Composition of Demospongiae from the Red Sea, Gulf of Aqaba'. PLOS ONE, 9 (4), pp. e95775.

Menzie, C. A., Southworth, B., Stephenson, G. & Feisthauer, N. (2008) 'The Importance of Understanding the Chemical Form of a Metal in the Environment: The Case of Barium Sulfate (Barite)'. Human and Ecological Risk Assessment: An International Journal, 14 (5), pp. 974-991.

1 comment:

  1. Hi Alessandro,

    Thank you for your post, it was very interesting. Did the authors mention what allows some bacterial symbionts to tolerate arsenic? Also, was there any benefit to the bacterial symbionts and the sponge cell fractions of concentrating arsenic and barium?

    Thank you
    Georgia

    ReplyDelete

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