Advertisement

Limnology

, Volume 19, Issue 2, pp 177–183 | Cite as

Diversity of anaerobic arsenite-oxidizing bacteria in low-salt environments analyzed with a newly developed PCR-based method

  • Melody Cabrera Ospino
  • Hisaya KojimaEmail author
  • Tomohiro Watanabe
  • Tomoya Iwata
  • Manabu Fukui
Rapid communication Note on important and novel findings

Abstract

Anaerobic arsenite oxidation is potentially important but the least understood process in the arsenic cycle. The catalytic subunit of the key enzyme for anaerobic arsenite oxidation is encoded by the arxA gene. In this study, a novel primer pair for the arxA gene was designed to detect diverse sequences of this notable gene. Further modification of the designed primer was made by adding extra bases to its 5′- end. This modification made it possible to analyze the PCR products with TA cloning, which provides higher throughput of investigations. With the combination of modified primer pair and TA cloning, diverse arxA gene sequences were effectively obtained from samples of lake water, spring water, and hot spring microbial mat. The sequences detected in the samples characterized by low salinity and nearly neutral pH were phylogenetically distinct from the majority of previously known arxA genes, found in the genome of alkaliphiles and halophiles.

Keywords

Arsenic Arsenite oxidase arxA PCR detection Primer design 

Notes

Acknowledgements

We are grateful to Arisa Shinohara for technical assistance. This work was supported by KAKENHI Grant Number 15K07209 to Kojima.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest.

Supplementary material

10201_2018_539_MOESM1_ESM.pdf (412 kb)
Supplementary material 1 (PDF 412 kb)
10201_2018_539_MOESM2_ESM.pdf (202 kb)
Supplementary material 2 (PDF 201 kb)

References

  1. Al Ait L, Yamak Z, Morgenstern B (2013) DIALIGN at GOBICS-multiple sequence alignment using various sources of external information. Nucleic Acids Res 41:3–7CrossRefGoogle Scholar
  2. Anantharaman K, Brown CT, Hug LA, Sharon I, Castelle C, Probs AJ, Thomas BC, Singh A, Wilkins MJ, Karaoz U et al (2016) Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat Commun 7:1–11CrossRefGoogle Scholar
  3. Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55:539–552CrossRefPubMedGoogle Scholar
  4. Costa PS, Scholte LLS, Reis MP, Chaves AV, Oliveira PL, Itabayana LB, Suhadolnik MLS, Barbosa FAR, Chartone-Souza E, Nascimento AMA (2014) Bacteria and genes involved in arsenic speciation in sediment impacted by long-term gold mining. PLoS ONE 9:1–12Google Scholar
  5. Fernández-Llamosas H, Prandoni N, Fernández-Pascual M, Fajardo S, Morcillo C, Diaz E, Carmona M (2014) Azoarcus sp. CIB, an anaerobic biodegrader of aromatic compounds shows an endophytic lifestyle. PLoS ONE 9:1–11Google Scholar
  6. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321CrossRefPubMedGoogle Scholar
  7. Hamamura N, Macur RE, Korf S, Ackerman G, Taylor WP, Kozubal M, Reysenbach AL, Inskeep WP (2009) Linking microbial oxidation of arsenic with detection and phylogenetic analysis of arsenite oxidase genes in diverse geothermal environments. Environ Microbiol 11:421–431CrossRefPubMedGoogle Scholar
  8. Hamamura N, Fukushima K, Itai T (2013) Identification of antimony- and arsenic-oxidizing bacteria associated with antimony mine tailing. Microbes Env 28:257–263CrossRefGoogle Scholar
  9. Hamamura N, Itai T, Liu Y, Reysenbach AL, Damdinsuren N, Inskeep WP (2014) Identification of anaerobic arsenite-oxidizing and arsenate-reducing bacteria associated with an alkaline saline lake in Khovsgol, Mongolia. Environ Microbiol Rep 6:476–482CrossRefPubMedGoogle Scholar
  10. Hernandez-Maldonado J, Sanchez-Sedillo B, Stoneburner B, Boren A, Miller L, Mccann S, Rosen M, Oremland RS, Saltikov CW (2017) The genetic basis of anoxygenic photosynthetic arsenite oxidation. Environ Microbiol 19:130–141CrossRefPubMedGoogle Scholar
  11. Hoeft McCann S, Boren A, Hernandez-Maldonado J, Stoneburner B, Saltikov C, Stolz J, Oremland R (2017) Arsenite as an electron donor for anoxygenic photosynthesis: description of three strains of Ectothiorhodospira from Mono Lake, California and Big Soda Lake, Nevada. Life 7:1–14CrossRefGoogle Scholar
  12. Hoeft SE, Blum JS, Stolz JF, Tabita FR, Witte B, King GM, Santini JM, Oremland RS (2007) Alkalilimnicola ehrlichii sp. nov., a novel, arsenite-oxidizing haloalkaliphilic gammaproteobacterium capable of chemoautotrophic or heterotrophic growth with nitrate or oxygen as the electron acceptor. Int J Syst Evol Microbiol 57:504–512CrossRefPubMedGoogle Scholar
  13. Hollibaugh JT, Budinoff C, Hollibaugh R, Ransom B, Bano N (2006) Sulfide oxidation coupled to arsenate reduction by a diverse microbial community in a soda lake. Appl Environ Microbiol 72:2043–2049CrossRefPubMedPubMedCentralGoogle Scholar
  14. Kojima H, Fukui M (2010) Sulfuricella denitrificans gen. nov., sp. nov., a sulfur-oxidizing autotroph isolated from a freshwater lake. Int J Syst Evol Microbiol 60:2862–2866CrossRefPubMedGoogle Scholar
  15. Kojima H, Iwata T, Fukui M (2009) DNA-based analysis of planktonic methanotrophs in a stratified lake. Freshw Biol 54:1501–1509CrossRefGoogle Scholar
  16. Kojima H, Watanabe T, Iwata T, Fukui M (2014) Identification of major planktonic sulfur oxidizers in stratified freshwater lake. PLoS ONE 9:1–7Google Scholar
  17. Kojima H, Watanabe M, Fukui M (2017) Sulfuritortus calidifontis gen. nov., sp. nov., a novel sulfur oxidizer isolated from a hot spring microbial mat. Int J Syst Evol Microbiol 67:1355–1358CrossRefPubMedGoogle Scholar
  18. Kulp TR, Hoeft SE, Asao M, Madigan MT, Hollibaugh JT, Fisher JC, Stolz JF, Culbertson CW, Miller LG, Oremland RS (2008) Arsenic(III) fuels anoxygenic photosynthesis in hot spring biofilms from Mono Lake, California. Science 321:967–970CrossRefPubMedGoogle Scholar
  19. Mandal BK, Suzuki KT (2002) Arsenic round the world: a review. Talanta 58:201–235CrossRefPubMedGoogle Scholar
  20. Martin-Moldes Z, Zamarro MT, del Cerro C, Valencia A, Gomez MJ, Arcas A, Udaondo Z, Garcia JL, Nogales J, Carmona M, Diaz E (2015) Whole-genome analysis of Azoarcus sp. strain CIB provides genetic insights to its different lifestyles and predicts novel metabolic features. Syst Appl Microbiol 38:462–471CrossRefPubMedGoogle Scholar
  21. Meyer-Dombard DR, Amend JP, Osburn MR (2013) Microbial diversity and potential for arsenic and iron biogeochemical cycling at an arsenic rich, shallow-sea hydrothermal vent (Tutum Bay, Papua New Guinea). Chem Geol 348:37–47CrossRefGoogle Scholar
  22. Probst AJ, Castelle CJ, Singh A, Brown CT, Anantharaman K, Sharon I, Hug LA, Burstein D, Emerson JB, Thomas BC, Banfield JF (2017) Genomic resolution of a cold subsurface aquifer community provides metabolic insights for novel microbes adapted to high CO2 concentrations. Environ Microbiol 19:459–474CrossRefPubMedGoogle Scholar
  23. Richey C, Chovanec P, Hoeft SE, Oremland RS, Basu P, Stolz JF (2009) Respiratory arsenate reductase as a bidirectional enzyme. Biochem Biophys Res Commun 382:298–302CrossRefPubMedGoogle Scholar
  24. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefPubMedPubMedCentralGoogle Scholar
  25. Shankar S, Shanker U, Shikha U (2014) Arsenic contamination of groundwater: a review of sources, prevalence, health risks, and strategies for mitigation. Sci World J 2014:1–18CrossRefGoogle Scholar
  26. Switzer Blum J, Hoeft McCann S, Bennett S, Miller LG, Stolz JR, Stoneburner B, Saltikov C, Oremland RS (2016) A microbial arsenic cycle in sediments of an acidic mine impoundment: Herman Pit, Clear Lake, California. Geomicrobiol J 33:677–689CrossRefGoogle Scholar
  27. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  28. Watanabe T, Kojima H, Takano Y, Fukui M (2013) Diversity of sulfur-cycle prokaryotes in freshwater lake sediments investigated using aprA as the functional marker gene. Syst Appl Microbiol 36:436–443CrossRefPubMedGoogle Scholar
  29. Watanabe T, Kojima H, Fukui M (2014) Complete genomes of freshwater sulfur oxidizers Sulfuricella denitrificans skB26 and Sulfuritalea hydrogenivorans sk43H: genetic insights into the sulfur oxidation pathway of betaproteobacteria. Syst Appl Microbiol 37:387–395CrossRefPubMedGoogle Scholar
  30. Watanabe T, Kojima H, Fukui M (2015) Draft genome sequence of a sulfur-oxidizing autotroph, Sulfuricella sp. strain T08, isolated from a freshwater lake. Genome Announc 3:8–9Google Scholar
  31. Watanabe T, Kojima H, Fukui M (2016) Sulfuriferula thiophila sp. nov., a chemolithoautotrophic sulfur-oxidizing bacterium, and correction of the name Sulfuriferula plumbophilus Watanabe, Kojima and Fukui 2015 to Sulfuriferula plumbiphila corrig. Int J Syst Evol Microbiol 66:2041–2045CrossRefPubMedGoogle Scholar
  32. Watanabe T, Miura A, Iwata T, Kojima H, Fukui M (2017) Dominance of Sulfuritalea species in nitrate-depleted water of a stratified freshwater lake and arsenate respiration ability within the genus. Environ Microb Rep 9:522–527CrossRefGoogle Scholar
  33. Zargar K, Hoeft S, Oremland R, Saltikov CW (2010) Identification of a novel arsenite oxidase gene, arxA, in the haloalkaliphilic, arsenite-oxidizing bacterium Alkalilimnicola ehrlichii strain MLHE-1. J Bacteriol 192:3755–3762CrossRefPubMedPubMedCentralGoogle Scholar
  34. Zargar K, Conrad A, Bernick DL, Lowe TM, Stolc V, Hoeft S, Oremland RS, Stolz J, Saltikov CW (2012) ArxA, a new clade of arsenite oxidase within the DMSO reductase family of molybdenum oxidoreductases. Environ Microbiol 14:1635–1645CrossRefPubMedGoogle Scholar

Copyright information

© The Japanese Society of Limnology 2018

Authors and Affiliations

  • Melody Cabrera Ospino
    • 1
    • 2
  • Hisaya Kojima
    • 1
    Email author
  • Tomohiro Watanabe
    • 1
    • 4
  • Tomoya Iwata
    • 3
  • Manabu Fukui
    • 1
  1. 1.The Institute of Low Temperature ScienceHokkaido UniversitySapporoJapan
  2. 2.Graduate School of Environmental ScienceHokkaido UniversitySapproJapan
  3. 3.Department of Environmental SciencesUniversity of YamanashiKofuJapan
  4. 4.Max Planck Institute for Terrestrial MicrobiologyMarburgGermany

Personalised recommendations