Extracellular DNA Can Preserve the Genetic Signatures of Present and Past Viral Infection Events in Deep Hypersaline Anoxic Basins

Overview

Journal Proc Biol Sci

Specialty Biology

Date 2014 Feb 14

PMID 24523277

Citations 20

Authors

C Corinaldesi

M Tangherlini

G M Luna

A DellAnno

Affiliations

Soon will be listed here.

Abstract

Deep hypersaline anoxic basins (DHABs) of the Mediterranean Sea are among the most extreme ecosystems on Earth and host abundant, active and diversified prokaryotic assemblages. However, factors influencing biodiversity and ecosystem functioning are still largely unknown. We investigated, for the first time, the impact of viruses on the prokaryotic assemblages and dynamics of extracellular DNA pool in the sediments of La Medee, the largest DHAB found on Earth. We also compared, in La Medee and L'Atalante sediments, the diversity of prokaryotic 16S rDNA sequences contained in the extracellular DNA released by virus-induced prokaryotic mortality. We found that DHAB sediments are hot-spots of viral infections, which largely contribute to the release of high amounts of extracellular DNA. DNase activities in DHAB sediments were much higher than other extracellular enzymatic activities, suggesting that extracellular DNA released from killed prokaryotes can be the most suitable trophic resource for benthic prokaryotes. Preserved extracellular DNA pools, which contained novel and diversified gene sequences, were very similar between the DHABs but dissimilar from the respective microbial DNA pools. We conclude that the strong viral impact in DHAB sediments influences the genetic composition of extracellular DNA, which can preserve the signatures of present and past infections.

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References

van der Wielen P, Bolhuis H, Borin S, Daffonchio D, Corselli C, Giuliano L . The enigma of prokaryotic life in deep hypersaline anoxic basins. Science. 2005; 307(5706):121-3. DOI: 10.1126/science.1103569. View

Tamburini C, Boutrif M, Garel M, Colwell R, Deming J . Prokaryotic responses to hydrostatic pressure in the ocean--a review. Environ Microbiol. 2013; 15(5):1262-74. DOI: 10.1111/1462-2920.12084. View

Schloss P, Westcott S, Ryabin T, Hall J, Hartmann M, Hollister E . Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009; 75(23):7537-41. PMC: 2786419. DOI: 10.1128/AEM.01541-09. View

Coolen M, Cypionka H, Sass A, Sass H, Overmann J . Ongoing modification of Mediterranean Pleistocene sapropels mediated by prokaryotes. Science. 2002; 296(5577):2407-10. DOI: 10.1126/science.1071893. View

Corinaldesi C, Beolchini F, DellAnno A . Damage and degradation rates of extracellular DNA in marine sediments: implications for the preservation of gene sequences. Mol Ecol. 2008; 17(17):3939-51. DOI: 10.1111/j.1365-294X.2008.03880.x. View

Antunes A, Alam I, El Dorry H, Siam R, Robertson A, Bajic V . Genome sequence of Haloplasma contractile, an unusual contractile bacterium from a deep-sea anoxic brine lake. J Bacteriol. 2011; 193(17):4551-2. PMC: 3165496. DOI: 10.1128/JB.05461-11. View

Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P . The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2012; 41(Database issue):D590-6. PMC: 3531112. DOI: 10.1093/nar/gks1219. View

Orsi W, Charvet S, Vdacny P, Bernhard J, Edgcomb V . Prevalence of partnerships between bacteria and ciliates in oxygen-depleted marine water columns. Front Microbiol. 2012; 3:341. PMC: 3446810. DOI: 10.3389/fmicb.2012.00341. View

Danovaro R, Corinaldesi C, DellAnno A, Fabiano M, Corselli C . Viruses, prokaryotes and DNA in the sediments of a deep-hypersaline anoxic basin (DHAB) of the Mediterranean Sea. Environ Microbiol. 2005; 7(4):586-92. DOI: 10.1111/j.1462-2920.2005.00727.x. View

10.

Akoumianaki I, Nomaki H, Pachiadaki M, Kormas K, Kitazato H, Tokuyama H . Low bacterial diversity and high labile organic matter concentrations in the sediments of the Medee deep-sea hypersaline anoxic basin. Microbes Environ. 2012; 27(4):504-8. PMC: 4103561. DOI: 10.1264/jsme2.me12045. View

11.

Coolen M, Orsi W, Balkema C, Quince C, Harris K, Sylva S . Evolution of the plankton paleome in the Black Sea from the Deglacial to Anthropocene. Proc Natl Acad Sci U S A. 2013; 110(21):8609-14. PMC: 3666672. DOI: 10.1073/pnas.1219283110. View

12.

Borin S, Brusetti L, Mapelli F, DAuria G, Brusa T, Marzorati M . Sulfur cycling and methanogenesis primarily drive microbial colonization of the highly sulfidic Urania deep hypersaline basin. Proc Natl Acad Sci U S A. 2009; 106(23):9151-6. PMC: 2685740. DOI: 10.1073/pnas.0811984106. View

13.

Corinaldesi C, Barucca M, Luna G, DellAnno A . Preservation, origin and genetic imprint of extracellular DNA in permanently anoxic deep-sea sediments. Mol Ecol. 2010; 20(3):642-54. DOI: 10.1111/j.1365-294X.2010.04958.x. View

14.

Rothschild L, Mancinelli R . Life in extreme environments. Nature. 2001; 409(6823):1092-101. DOI: 10.1038/35059215. View

15.

Cao H, Auguet J, Gu J . Global ecological pattern of ammonia-oxidizing archaea. PLoS One. 2013; 8(2):e52853. PMC: 3585293. DOI: 10.1371/journal.pone.0052853. View

16.

DellAnno A, Corinaldesi C . Degradation and turnover of extracellular DNA in marine sediments: ecological and methodological considerations. Appl Environ Microbiol. 2004; 70(7):4384-6. PMC: 444808. DOI: 10.1128/AEM.70.7.4384-4386.2004. View

17.

Lorenz M, Wackernagel W . Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev. 1994; 58(3):563-602. PMC: 372978. DOI: 10.1128/mr.58.3.563-602.1994. View

18.

Corinaldesi C, Danovaro R, DellAnno A . Simultaneous recovery of extracellular and intracellular DNA suitable for molecular studies from marine sediments. Appl Environ Microbiol. 2005; 71(1):46-50. PMC: 544275. DOI: 10.1128/AEM.71.1.46-50.2005. View

19.

Sass A, Sass H, Coolen M, Cypionka H, Overmann J . Microbial communities in the chemocline of a hypersaline deep-sea basin (Urania basin, Mediterranean Sea). Appl Environ Microbiol. 2001; 67(12):5392-402. PMC: 93321. DOI: 10.1128/AEM.67.12.5392-5402.2001. View

20.

DellAnno A, Danovaro R . Extracellular DNA plays a key role in deep-sea ecosystem functioning. Science. 2005; 309(5744):2179. DOI: 10.1126/science.1117475. View