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Extracellular DNA Plays a Key Role in Deep-Sea Ecosystem Functioning

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Science  30 Sep 2005:
Vol. 309, Issue 5744, pp. 2179
DOI: 10.1126/science.1117475

Abstract

The ecological role and biogeochemical relevance of extracellular DNA in the oceanic sediments are unknown. Our global estimates indicate that up to 0.45 gigatons of extracellular DNA are present in the top 10 centimeters of deep-sea sediments, representing the largest reservoir of DNA in the world oceans. We demonstrate that extracellular DNA accounts for about one fifth of the total organic phosphorus regeneration and provides almost half of the prokaryotic demand for organic phosphorus. It therefore plays a key role in deep-sea ecosystem functioning on a global scale.

The regeneration of phosphates from the organic P pool is a key step in the regulation of P availability in the oceans (1). However, the reason why organic P is preferentially recycled in the deep ocean, where phosphates are not limiting, has yet to be clarified. This limits our understanding of the P cycle and ecosystem functioning on a global scale (2).

DNA is a P-rich molecule (10% weight to weight), but the role of DNA in P cycling has largely been ignored to date, as it is typically viewed only as the genetic material associated with living biomass (3). Here we provide evidence that DNA concentrations in deep-sea sediments worldwide are extremely high (0.31 ± 0.18 g of DNA m–2 in the top centimeter) (4) and that more than 90% of the DNA in these sediments is extracellular. We first estimated the extracellular DNA fraction by calculating the difference between total DNA and the DNA within living biomass, determined by synoptic determinations on virus, prokaryote, unicellular eukaryote (protozoan), and small metazoan (meiofauna) abundances. Another approach, conducted with a nuclease-based procedure that degrades only the extracellular DNA, supports this finding, revealing that 60 ± 4% of the total DNA pool is enzymatically digestible (4).

Additional polymerase chain reaction and dot blot analyses demonstrated that extracellular DNA estimates were not biased by the DNA released from living biomass during recovery (4). Our worldwide estimates indicate that the DNA content in the uppermost 10 cm of the deep-sea sediments is 0.50 ± 0.22 Gt. Therefore, extracellular DNA in deep-sea sediments (0.30 to 0.45 Gt) represents the largest reservoir of DNA in the world ocean. This amount is six- to eightfold higher than that of DNA contained in all benthic prokaryotes inhabiting the top 10 cm of the world marine sediments (5).

Pelagic-benthic coupling processes control the extracellular DNA distribution in world ocean sediments. This is suggested by the relationships between (i) DNA and phytopigment fluxes (Fig. 1A); (ii) DNA and phytopigment concentrations in surface sediments (Fig. 1B); and (iii) downward fluxes of DNA and sedimentary extracellular DNA content (Fig. 1C). The input of DNA from the photic layer to the deep sea stimulates the production of benthic prokaryotes, which represent ∼90% of the total biomass (6). Our estimates indicate that the total DNA input to the sea floor is 1.26 ± 0.18 × 107 metric tons year–1 and that extracellular DNA accounts for 13% of the total organic P flux (9.91 × 106 metric tons year–1, below 1000 m in depth) (7) to the deep sea.

Fig. 1.

(A) The relationship between DNA and phytopigment fluxes. Data are from the Atlantic Ocean at 3000 m and 4700 m in depth (green and yellow dots, respectively). d, day. (B) The relationship between total DNA and phytopigment content in the sediments. Data are from the Atlantic (red), Pacific (azure), Indian (green), and Southern (dark blue) oceans and the Mediterranean Sea (yellow). (C) The relationship between sedimentary extracellular DNA concentrations and DNA fluxes. Data are from the Atlantic Ocean (red) and the Eastern Mediterranean Sea (yellow).

We calculated that the contribution of the P associated with extracellular DNA to the total organic P pool is ∼3% (giving a global projection of 0.4 Gt of organic P) and that the residence time, in the top centimeter, is 40.3 years for organic P and 9.5 years for DNA. The measurements of high deoxyribonuclease activities (0.50 ± 0.15 mg of DNA m–2 day–1) (3) provide more direct evidence that the extracellular DNA pool can substantially contribute to P cycling. The application of a diagenetic model allowed us to estimate that extracellular DNA remineralization in the top 10 cm of the sediment accounts for 17% of the total organic P regeneration (range, 14 to 21%) (4). All of these findings indicate that the extracellular DNA in deep-sea sediments is selectively remineralized within the organic P pool and rapidly degraded.

Life in the deep-sea sediments is largely dominated by prokaryotes (8). Extracellular DNA, being a suitable C and N source (4), is important for deep-sea benthic prokaryote metabolism. Using synoptic measurements (4), we calculated that the use of extracellular DNA alone supplies 4, 7, and 47% of daily prokaryotic C, N, and P demand, respectively. Therefore, the use of a labile C and N source found in extracellular DNA results in fast P regeneration.

Our findings indicate that the availability of extracellular DNA can have profound implications on deep-sea ecosystem functioning, contributing substantially to P cycling and representing a key trophic resource.

Supporting Online Material

www.sciencemag.org/cgi/content/full/309/5744/2179/DC1

Materials and Methods

Figs. S1 to S3

Tables S1 to S3

References and Notes

References and Notes

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