Jaime Hernandez Discovers How Microbes Use Arsenic to Fuel an Unusual Form of Photosynthesis

November 21, 2016

Photoarsenotrophy

Jaime Hernandez-Maldonado, Ph.D. student in METX in the Saltikov Lab, recently discovered how microbes use the toxic compound arsenic to fuel an unusual form of photosynthesis1. In contrast to how plants split water into oxygen during their photosynthesis, anoxygenic photosynthetic arsenite oxidizing microbes “split” arsenic. This split form is less toxic and more likely to be retained in soils. This is good news for preventing arsenic pollution, because tens of millions of people in countries such as Argentina, Mexico, Chile, Cambodia, Vietnam, India, and Bangladesh depend on water sources high in arsenic.

Anoxygenic photosynthetic arsenite oxidizing microbes—also called photoarsenotrophs for their light and arsenic-loving properties—were first isolated from red-colored microbial mats within hot pools of Paoha Island, Mono Lake, California, an arsenic-rich extreme alkaline hypersaline lake2 (Fig. A). Since their discovery, questions remained about the mechanism for sunlight-dependent microbial metabolism that is fueled by arsenite. This was a challenging question to address due to the lack of a suitable photoarsenotroph that could be manipulated for genetic studies. The Saltikov Lab was poised to overcome this challenge because they had isolated a photoarsenotrophic bacterium called Ectothiorhodospira sp. strain BSL-9 that was genetically manipulable (Fig. B). Jaime identified a cluster of genes, and based on their sequences,  hypothesized they would encode enzymes necessary for photosynthetic arsenite oxidation. Having the genome sequence in hand and developing a genetic system in Ectothiorhodospira sp BSL-93, Jaime was equipped with the tools needed to disrupt the main gene, arxA. He demonstrated through bacterial physiology experiments that indeed his hypothesis was correct: He had discovered a new gene cluster required for photoarsenotrophy.

Jaime then headed a team from UCSC and the US Geological Survey to investigate whether these microbes are active in the environment, by detecting arxA mRNA in samples collected from the hot springs of Paoha Island, dominated by Ectothiorhodospira bacteria (Fig. A). The arxA mRNA would only be found in bacteria that are undergoing active arsenite oxidation in the environment, demonstrating that this process occurs in the real world.

The work of Jaime and his colleagues has established—for the first time—the critical genes responsible for sunlight-dependent arsenite microbial metabolism. It furthermore provides evidence that photoarsenotrophic growth occurs in arsenic rich extreme environments. Now we can further investigate photoarsenotrophy in other environments rich in arsenic such as those found in Argentina, Mexico, Chile, Cambodia, Vietnam, India, and Bangladesh. Eventually, this work may allow us to modulate the form of arsenic found in drinking water, and ultimately, its toxicity.

References

  1. J Hernandez-Maldonado, B Sanchez-Sedillo, B Stoneburner, A. Boren, L Miller, S McCann, M Rosen, R S. Oremland, C W. Saltikov (2016).  The genetic basis of anoxygenic photosynthetic arsenite oxidation.  Environ. Microbiol.  DOI: 10.1111/1462-2920.13509
  2. Kulp, T.R., Hoeft, S.E., Asao, M., Madigan, M.T., Hollibaugh, J.T., Fisher, J.C., et al. (2008) Arsenic(III) Fuels Anoxygenic Photosynthesis in Hot Spring Biofilms from Mono Lake, California. Science 321: 967–970.
  3. J Hernandez-Maldonado, B Stoneburner, A Boren, L Miller, S McCann, M Rosen, R S. Oremland, C W. Saltikov (2016).  Genome sequence of Ectothiorhodospira sp. Strain BSL-9, an anoxygenic photosynthetic arsenite oxidizing purple sulfur bacterium.  Genome Announc.  DOI: 10.1128/genomeA.01139-16