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Geomicrobiology

Researchers investigate how microbes interact with the nonliving parts of Earth such as soils, sediment, and atmosphere.

Microbiology

Arsenic

Browse samples of USGS research about geomicrobiology and arsenic. For related links, see Related Links and References at the bottom of page.

Alkalilimnicola ehrlichii strain MLHE-1, a chemoautotrophic As(III)- oxidizer that respires nitrate, isolated by S. Hoeft from anoxic Mono Lake water.

Arsenic Geomicrobiology (Oremland)

A “red mat” biofilm in a hot spring on Paoha Island in Mono Lake

Arsenic Biochemistry (Oremland)

Satellite image of Mono Lake

Arsenic Biogeochemistry (Oremland)

Tufa towers in Mono Lake. Photo credit: USGS.

Arsenic Biogeochemistry (Oremland)


Arsenic Geomicrobiology
Photo: Researchers Ronald Oremland and Felisa Wolfe-Simon examine a mud sample from Mono Lake. Credit: Henry Bortman, Science/AAAS
Photo: Researchers Ronald Oremland and Felisa Wolfe-Simon examine a mud sample from Mono Lake. Credit: Henry Bortman, Science/AAAS.
tufa towers in Mono Lake
Tufa towers in Mono Lake. Photo credit: USGS.

Researchers in Dr. Ron Oremland’s USGS laboratory in Menlo, Park, California have just discovered a new way to look at and for possible extraterrestrial life. Oremland had previously discovered bacteria in the hypersaline, alkaline,  arsenic-rich Mono Lake in eastern California, that use the usually toxic element in photosynthesis, chemo-autotrophy,  or anaerobic respiratory reactions,  However, it had not been demonstrated that an organism could take up arsenic for internal use to drive cell metabolism. Last year, Dr. Felisa Wolfe-Simon joined Oremland’s lab, supported by a NASA Astrobiology fellowship. She proposed to determine whether arsenic, in the form of the arsenate ion, could be substituted for phosphate ions inside the bacterial cell.  To achieve this, the researchers inoculated sediments from Mono Lake into a growth medium, which contained arsenic but not phosphorus.  They were able to isolate a strain of bacteria (GFAJ-1) that grows in arsenate-rich or phosphate-rich conditions but does not grow when deprived of both arsenate and phosphate.  

This is a real breakthrough as previously we have recognized six elements that sustain life (carbon, hydrogen, nitrogen, oxygen, phosphorus and sulfur) to which we now, in some cases, may add arsenic.  Once these initial results were obtained at the USGS, they engaged collaborating colleagues at other institutions (ASU, LLNL, SLAC, Duquesne University) who employed a diversity of analytical tools (e.g., x-ray spectroscopy, nano-SIMS, ICP-mass spectroscopy, electron microscopy) in addition to radioisotope tracers work conducted at USGS to confirm that arsenate was incorporated into internal biomolecules, including the backbone of DNA, a slot usually occupied by phosphate.

Additional Links:

For more information contact Ronald S. Oremland, Menlo Park Regional Office.

 

 

Arsenic Geomicrobiology
Alkalilimnicola ehrlichii strain MLHE-1, a chemoautotrophic As(III)- oxidizer that respires nitrate, isolated by S. Hoeft from anoxic Mono Lake water. Fig. 1.
Strain MLMS-1, an obligate As(V) respirer isolated from anoxic Mono Lake water by S. Hoeft
Fig. 2.
Bacillus arseniciselenatis, isolated from Mono Lake sediments by J. Switzer Blum. Fig. 3.
Halarsenatibacter silvermanii, an anaerobic extremophile isolated by J. Switzer Blum from the sediments of salt-saturated, arsenic-rich Searles Lake.
Fig. 4.
Phylogenetic diversity of DARPs (blue dots) and CAOs (red squares), and heterotrophic arsenite oxidizers (gold triangles; not complete) as compiled by Oremland and Stolz (2003) and recently updated (Oremland et al., 2009). Fig. 5. Larger View
Phylogenetic diversity of DARPs (blue dots) and CAOs (red squares), and heterotrophic arsenite oxidizers (gold triangles; not complete) as compiled by Oremland and Stolz (2003) and recently updated (Oremland et al., 2009).

The arsenic oxyanions arsenate [As(V)] and arsenite [As(III)] have been known to be potent poisons for millennia. Yet a number of microorganisms from the Bacteria and Archaea Domains can employ these oxyanions to sustain their growth, either by carrying out the anaerobic respiratory reduction of As(V) to As(III), or conversely using As(III) as an electron donor for autotrophic growth. Starting with the identification of two closely related members of the ε-Proteobacteria in the genus Sulfurospirillum in the mid-1990s, now over 20 species of dissimilatory arsenate respiring prokaryotes (DARPs) have been isolated, many of them in our lab. Phylogenetically they are highly diverse, while in contrast, aerobic chemoautrophic As(III)-oxidizers (CAOs) are much more constrained (see below figure). One unusual microorganism, Alkalilimnicola ehrlichii, is able to grow as a chemoautotroph (CAO) by linking As(III) oxidation to nitrate reduction rather than oxygen.

View related publications at Related Links and References.

For more information contact Ronald S. Oremland, Menlo Park Regional Office.

 

 

Examples of Microbes that Grow by Coupling Arsenic Metabolism to Energy Conservation:
Figure 1. Alkalilimnicola ehrlichii strain MLHE-1, a chemoautotrophic As(III)- oxidizer that respires nitrate, isolated by S. Hoeft from anoxic Mono Lake water. It can also grow in this mode with hydrogen or sulfide in lieu of As(III). This microbe can also grow as an aerobic heterotroph on acetate, and its full genome has been sequenced and annotated (Hoeft et al., 2002; Oremland et al., 2002; Hoeft et al., 2007).
Figure 2. Strain MLMS-1, an obligate As(V) respirer isolated from anoxic Mono Lake water by S. Hoeft. This microorganisms is also an obligate chemoautotroph that uses sulfide as its electron donor to respire As(V). (Hoeft et al., 2004).
Figure 3. Bacillus arseniciselenatis, isolated from Mono Lake sediments by J. Switzer Blum. This anaerobe is a heterotroph that uses lactate as its electron donor and is capable of using a number of electron acceptors for respiration, including arsenate, selenate, tellurate, fumarate, and nitrate (Switzer Blum et al., 1998; Baesman et al., 2008).
Figure 4. Halarsenatibacter silvermanii, an anaerobic extremophile isolated by J. Switzer Blum from the sediments of salt-saturated, arsenic-rich  Searles Lake. This microbe is an anaerobe that can grow either as a heterotroph using lactate as its electron donor or as a chemo-autotroph using sulfide in that role (Oremland et al., 2005; Switzer Blum et al., 2009).

Arsenic Biochemistry
A “red mat” biofilm in a hot spring on Paoha Island in Mono Lake. Fig. 1.
Incubation of scraped mat material under anaerobic conditions in the light resulted in the oxidation of As(III) to As(V)
Fig. 2. Larger View
Unrooted neighbor-joining tree of representative protein sequences of the DMSO reductase family of molybdenum oxidoreductases (from Oremland et al., 2009)Fig. 3. Larger View
The microbial cycle of arsenic in nature showing a coupling between As(V) reductive process on the right hand side and the As(III) oxidative processes on the left hand side
Fig. 4. Larger View
Possible time-line origin of As(III) anoxygenic photosynthesis preceding the appearance of atmospheric oxygen
Fig. 5. Larger View

All DARPs contain an arsenate reductase (ArrAB), a heterodimeric Mo-containing enzyme located in the outer cell envelope (e.g., periplasm).There is diversity in the gene sequences of the arrA components amongst species of known As(V)-respirers, many of which have undergone full genome sequencing and annotation. Curiously, the genome of the anaerobic CAO A. ehrlichii strain MLHE-1 lacks an As(III) oxidase (aoxBA), but instead contains two arrA-type genes. Richey et al. (2009) demonstrated that the arsenate reductase of strain MLHE-1 is running in reverse in vivo and essentially functioning as an oxidase.

Recently, we reported that photosynthetic bacteria located in hot springs in Mono Lake were capable of using As(III) as their electron donor to drive anoxygenic photosynthesis (Kulp et al., 2008). A pure culture of a γ-Proteobacterium, Ectothiorhodospira strain PHS-1, was isolated by S. Hoeft and demonstrated As(III) dependent growth in the light. This organism also lacks an As(III) oxidase, but contains an As(V) reductase very similar to that of A. ehrlichii, and presumably functioning in vivo as an As(III) oxidase.

This allows us to speculate on when As(V) respiration on Earth first arose. The high phylogenetic diversity of DARPs could reflect a long period of vertical evolution with concomitant radiation over time. Oxidation of As(III) emanating from the early Earth’s volcanic sources could be oxidized to As(V) by photosynthetic bacteria, allowing for the creation of niches for DARPs well before the Great Oxidation Event (~ 2.4 Ga) possibly as far back as 3.4 Ga.

View related publications at Related Links and References.

For more information contact Ronald S. Oremland, Menlo Park Regional Office.

Figure 1/2. A “red mat” biofilm in a hot spring on Paoha Island in Mono Lake (top panel). Incubation of scraped mat material under anaerobic conditions in the light resulted in the oxidation of As(III) to As(V) (bottom panel) (from Kulp et al., 2008).
Figure 3. Unrooted neighbor-joining tree of representative protein sequences of the DMSO reductase family of molybdenum oxidoreductases (from Oremland et al., 2009). Grey shaded areas represent clades for the arsenate respiratory reductase and arsenite oxidase.  The Genbank accession numbers are listed at the end of the organisms’ names. Text within the parenthesis indicates the location of the particular DNA coding sequence within the genome sequence of the particular organism.  Numerical superscripts indicate species identified by physiological tests that can grow by respiring As(V)1 or can oxidize As(III)2.
Figure 4. The microbial cycle of arsenic in nature showing a coupling between As(V) reductive process on the right hand side and the As(III) oxidative processes on the left hand side. The discovery of As(III)-fueled anoxygenic photosynthesis allows for the regeneration of As(V) without the need to invoke the presence of strong oxidants (e.g., oxygen, nitrate) in the crust of the early Earth.
Figure 5. Possible time-line origin of As(III) anoxygenic photosynthesis preceding the appearance of atmospheric oxygen.

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Arsenic Biogeochemistry
Satellite image of Mono Lake Fig. 1.
Collecting mud through the salt crust of Searles Lake
Fig. 2.
Examples of some affected individuals from Bangladesh exhibiting clear symptoms of arsenicosis, as exemplified by disfiguring keritosis and painful skin lesions. Fig. 3.

While arsenic is a well-known poison utilized as a means to achieve homicide, or as a pesticide/herbicide, a current human health problem has arisen globally with regard to ingesting arsenic-containing groundwater. Over the course of years this can lead to the outbreak of arsenicosis initially presented as skin keritosis (see Fig. 3), lesions, and ultimately leading to the death of the affected individuals through multiple cancers and organ failure.

Microbes are involved in this process because they can mobilize adsorbed As(V) from the solid phase into the aqueous phase of well water (e.g., Zobrist et al., 2000). To gain a better understanding of this process, we have conducted investigations of arsenic cycling in As-rich ecosystems, which are typified by being highly saline and alkaline as well. One such field site is Mono Lake, California, where DARPs were shown to be responsible for mineralizing about 14 % of autocthonous carbon derived from sinking phytoplankton (Oremland et al., 2000). While Mono Lake is an example of an environmental extreme (pH = 9.8; salinity = 90 g/L), we also investigated the arsenic cycle in another soda lake, namely Searles Lake (pH = 9.8; salinity = 340 g/L) in the Mohave Desert.

View related publications at Related Links and References.

For more information contact Ronald S. Oremland, Menlo Park Regional Office.

Figure 1/2. Satellite image of Mono Lake (top) and collecting mud through the salt crust of Searles Lake (bottom). The arsenic content of Mono is 200 μM, while that of Searles is 4 mM. The sediments from both ecosystems have an active microbial arsenic cycle (Oremland et al., 2005; Kulp et al., 2006; Kulp et al., 2007)
Figure 3. Examples of some affected individuals from Bangladesh exhibiting clear symptoms of arsenicosis, as exemplified by disfiguring keritosis and painful skin lesions.

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Related Links and References

Geomicrobiology, Biochemistry, and Biogeomicrobiology:

  • Laverman, A.M., J. Switzer Blum, J.K. Schaeffer, E.J. Philips, D.R. Lovley, and R.S. Oremland. 1995. Growth of strain SES-3 with arsenate and other diverse electron acceptors. Appl. Environ. Microbiol. 61: 3556 - 3561.
  • Dowdle, P.R., A.M. Laverman, and R.S. Oremland. 1996. Bacterial dissimilatory reduction of arsenic (V) to arsenic (III) in anoxic sediments. Appl. Environ. Microbiol. 62: 1664 - 1669.
  • Stolz, J.F., T. Gugliuzza, J. Switzer Blum, R.S. Oremland, and F.M. Murillo. 1997. Differential expression of cytochromes and reductases in Geospirillum barnesii strain SES3. Arch. Microbiol. 167: 1-5.
  • Switzer Blum, J., A. Burns Bindi, J. Buzzelli, J.F. Stolz, and R.S. Oremland. 1998. Bacillus arsenicoselenatis sp. nov., and Bacillus selenitireducens sp. nov. : two haloalkaliphiles from Mono Lake, California which respire oxyanions of selenium and arsenic. Arch. Microbiol. 171: 19 – 30.
  • Stolz, J.F., D.J. Ellis, J. Switzer Blum, D. Ahmann, R.S. Oremland, and D.R. Lovley.  1999. Sulfurospirillum barnesii sp. nov., Sulfurospirillum arsenophilus sp. nov., and the Sulfurospirillum clade in the Epsilon Proteobacteria. Int. J. Systematic Bacteriol. 49: 1177 - 1180.
  • Stolz, J.F., and R.S. Oremland. 1999. Bacterial respiration of selenium and arsenic. FEMS Microbiology Reviews, 23: 615 - 627.
  • Oremland, R.S., and J.F. Stolz. 2000. Dissimilatory reduction of selenate and arsenate in nature. p. 199 – 224 In D.R. Lovley (ed) Environmental Metal-Microbe Interaction, Amer. Soc. Microbiology Press, Washington, D.C.
  • Oremland, R.S., P.R. Dowdle, S. Hoeft, J.O. Sharp, J.K. Schaefer, L.G. Miller, J. Switzer Blum, R.L. Smith, N.S. Bloom, and D. Wallschlaeger. 2000. Bacterial dissimilatory reduction of arsenate and sulfate in meromictic Mono Lake, California. Geochim. Cosmochim. Acta 64: 3073 – 3084.
  • Zobrist, J., P.R. Dowdle, J.A. Davis, and R.S. Oremland. 2000. Mobilization of arsenite by dissimilatory reduction of adsorbed arsenate. Environ. Sci. Technol. 34: 4747 - 4753.
  • Oremland, R.S., D.K. Newman, B.W. Kail, and J.F. Stolz. 2001. Bacterial respiration of arsenate and its significance in the environment. p. 273 – 296 in W.T. Frankenberger Jr. (ed), Environmental Chemistry of Arsenic, Marcel Dekker, New York.
  • Herbel, M.J., J. Switzer Blum, S.E. Hoeft, S.M. Cohen, L.L. Arnold, J. Lisak, J.F. Stolz, and R.S. Oremland. 2002. Dissimilatory arsenate reductase activity and arsenate-respiring bacteria in bovine rumen fluid, hamster feces, and the termite hindgut. FEMS Microbiology Ecology 41: 59 – 67.
  • Oremland, R.S., S.E. Hoeft, N. Bano, R.A. Hollibaugh, and J.T. Hollibaugh. 2002 Anaerobic oxidation of arsenite in Mono Lake water and by a facultative, arsenite-oxidizing chemoautotroph, strain MLHE-1. Appl. Environ. Microbiol. 68: 4795 – 4802.
  • Oremland, R.S., and J.F. Stolz. 2003. The ecology of arsenic. Science 299: 939 - 944. Afkar, E., J. Lisak, C. Saltikov, P. Basu, R.S. Oremland, and J.F. Stolz. 2003. The respiratory arsenate reductase from Bacillus selenitireducens strain MLS10. FEMS Microbiology Lett. 226: 107 - 112.
  • Oremland, R.S., J.F. Stolz, and J.T. Hollibaugh. 2004. The microbial arsenic cycle in Mono Lake, California. FEMS Microbiology Ecology 48: 15 - 27.
  • Hoeft, S.E., T.R. Kulp, J.F. Stolz, J.T. Hollibaugh, and R.S. Oremland. 2004. Dissimilatory arsenate reduction with sulfide as the electron donor: Experiments with Mono Lake water and isolation of strain MLMS-1, a chemoautotrophic arsenate-respirer. Appl. Environ. Microbiol. 70: 2741 - 2747.
  • Kulp, T.R., S.E. Hoeft, and R.S. Oremland. 2004. Redox transformations of arsenic oxyanions in periphyton communities. Appl. Environ. Microbiol. 70: 6428 - 6434.
  • Oremland, R.S., and J.F. Stolz. 2005. Arsenic, microbes, and contaminated aquifers. Trends in Microbiology 13: 45 - 49.
  • Oremland, R.S., T.R. Kulp, J. Switzer Blum, S.E. Hoeft, S. Baesman, L.G. Miller, and J.F. Stolz. 2005. A microbial arsenic cycle in a salt-saturated, extreme environment. Science 308: 1305 – 1308.
  • Lloyd, J.R. and R.S. Oremland. 2006.  Microbial transformations of arsenic in the environment: From soda lakes to aquifers. Elements 2: 85 - 90.
  • Stolz, J.F., P. Basu, J.M. Santini and R.S. Oremland. 2006. Arsenic and selenium in microbial metabolism. Ann. Rev. Microbiology 60: 107 – 130.
  • Kulp, T.R., S.E. Hoeft, L.G. Miller, C. Saltikov, J. Nilsen, S. Han, B. Lanoil, and R.S. Oremland. 2006. Dissimilatory arsenate- and sulfate-reduction in sediments of two hypersaline, arsenic-rich soda lakes: Mono and Searles Lakes, California. Appl. Environ. Microbiol. 72: 6514 - 6526.
  • Hoeft, S.E., J. Switzer Blum, J.F. Stolz, F. R. Tabita, B. Witte, G.M. King, J.M. Santini, and R.S. Oremland. 2007. Alkalilimnicola ehlichii, sp. nov., a novel, arsenite-oxidizng haloalklapihilic γ-Proteobacterium capable of chemoautotrophic or heterotrophic growth with nitrate or oxygen as the electron acceptor. Int. J. Syst. Evol. Microbiol. 57: 504 - 512.
  • Kulp, T.R., S. Han, C. Saltikov, B. Lanoil, K. Zargar, and R.S. Oremland. 2007. Effects of imposed salinity gradients on dissimilatory arsenate-reduction, sulfate-reduction, and other microbial processes in sediments from two California soda lakes. Appl. Environ. Microbiol. 73: 5130 - 5137.
  • Kulp, T.R., S. E. Hoeft, M. Asao, M. T. Madigan, J. T. Hollibaugh, J. C. Fisher, J.F. Stolz, C.W. Culbertson, L.G. Miller, and R.S. Oremland. 2008. Arsenic(III) fuels anoxygenic photosynthesis in hot spring biofilms from Mono Lake, California. Science 321: 967 - 970.
  • Switzer Blum, J., S. Han, Brian Lanoil, C. Saltikov, B. Witte, F. R. Tabita, S. Langley, T. J. Beveridge, John F. Stolz, L. Jahnke and R.S. Oremland. 2009. Halarsenatibacter silvermanii strain SLAS-1T, gen. nov., sp. nov., ecophysiology of an extremely halophilic, facultative chemo-autotrophic arsenate-respirer of the Halanaerobiales isolated from Searles Lake, California. Appl. Environ. Microbiol. 75: 1950 - 1960.
  • Richey, C., P. Chovanec, S. Hoeft, R.S. Oremland, P. Basu, and J. F. Stolz. 2009. Respiratory arsenate reductase as a bidirectional enzyme. Biochem. Biophys. Res. Comm. 382: 298 - 302.
  • R.S. Oremland, F. Wolfe-Simon, C.W. Saltikov, and J.F. Stolz. 2009. Arsenic in the evolution of earth and extraterrestrial ecosystems. Geomicrobiology Journal,26:7,522 — 536, doi: 10.1080/01490450903102525 (on-line abstract of journal articleExternal link)
  • Sun, W., R. Sierra-Alvarez, L. Milner, R.S. Oremland, and J.A. Field. Arsenite and ferrous iron oxidation linked to chemolithotrophic denitrification for the immobilization of arsenic in anoxic environments. Environ. Sci. Technol. 45: 6585 - 6591. (online abstract of journal articleExternal link)

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