Our results indicate that gene loops act to
maintain the directionality of transcription. The
loss of a mammalian gene’s PAS can directly
influence the recruitment of transcription factors, with a consequent reduction in gene expression (22). PAS mutation has also been shown to
increase levels of divergent transcripts (23). On
the basis of our results, such effects are directly
explicable by the loss of gene-loop formation and
the potential to recycle factors from the terminator back to the promoter (see model, Fig. 4D).
The role of Rpd3S in restricting antisense terminator transcripts (Fig. 3) clearly illustrates the
importance of histone deacetylation in preventing
inappropriate ncRNA synthesis. We predict that
gene loops may similarly act to influence the recruitment of 5′ localized histone deacetylases
such as Set3 (24). This would maintain promoters in a deacetylated, inactive state until gene activation selectively promotes transcription of genes
rather than divergent pSRTs. We postulate that
gene looping contributes to determining which
transcription units are fully productive.
References and Notes
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12. D. W. Zhang et al., J. Biol. Chem. 287, 8541 (2012).
13. D. L. Pappas Jr., M. Hampsey, Mol. Cell. Biol. 20,
14. E. J. Steinmetz, D. A. Brow, Mol. Cell. Biol. 23, 6339
15. D. K. Pokholok et al., Cell 122, 517 (2005).
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17. S. C. Murray et al., Nucleic Acids Res. 40, 2432
18. M. J. Carrozza et al., Cell 123, 581 (2005).
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20. K. J. Perkins, M. Lusic, I. Mitar, M. Giacca, N. J. Proudfoot,
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21. A. G. Rondón, H. E. Mischo, J. Kawauchi, N. J. Proudfoot,
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22. C. K. Mapendano, S. Lykke-Andersen, J. Kjems,
E. Bertrand, T. H. Jensen, Mol. Cell 40, 410 (2010).
23. P. Preker et al., Nucleic Acids Res. 39, 7179 (2011).
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Acknowledgments: We thank B. Dichtl and J. Kufel for
strains and H. Wijayatilake for FMP27 and b-globin 3C
reagents. This work was supported by the Wellcome Trust
(N.J.P.), the NIH and Deutsche Forschungsgemeinschaft
(L.M.S.), European Molecular Biology Laboratory (J.B.Z.,
N.M.L., L.M.S.), and the Swiss National Fonds and European
Molecular Biology Organization (J.C.). Genomic data are
deposited at http://steinmetzlab.embl.de/proudfoot_
lab/ index.html (E-TABM-936).
Materials and Methods
Figs. S1 to S6
Tables S1 to S8
7 May 2012; accepted 14 September 2012
Published online 27 September 2012;
Trade-Offs of Chemotactic
John R. Taylor1 and Roman Stocker2*
Bacteria play an indispensable role in marine biogeochemistry by recycling dissolved organic
matter. Motile species can exploit small, ephemeral solute patches through chemotaxis and thereby
gain a fitness advantage over nonmotile competitors. This competition occurs in a turbulent
environment, yet turbulence is generally considered inconsequential for bacterial uptake. In
contrast, we show that turbulence affects uptake by stirring nutrient patches into networks of
thin filaments that motile bacteria can readily exploit. We find that chemotactic motility is subject
to a trade-off between the uptake benefit due to chemotaxis and the cost of locomotion, resulting
in an optimal swimming speed. A second trade-off results from the competing effects of stirring
and mixing and leads to the prediction that chemotaxis is optimally favored at intermediate
The average milliliter of seawater contains a million heterotrophic bacteria that play an essential role in remineralizing dissolved
organic matter (DOM) by decomposing 35 to
80% of net primary production (1) and converting
it into particulate form, available for consumption
by larger organisms. Most marine environments
are turbulent, ranging from the energetic mixed-layer and surf zone to calmer thermoclines, yet
the effect of turbulence on bacterial uptake of
DOM has remained elusive. This is due in part
to the difficulty of quantifying the microscale
biogeochemical variability generated by turbu-
1Department of Applied Mathematics and Theoretical Physics,
University of Cambridge, Wilberforce Road, Cambridge CB3
0WA, UK. 2Ralph M. Parsons Laboratory, Department of Civil
and Environmental Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA.
*To whom correspondence should be addressed. E-mail:
lence. At the same time, the physics of transport
at micrometer scales dictates that DOM uptake
occurs primarily by diffusion of nutrient molecules to cells (2). In a homogeneous nutrient
environment, marine turbulence is insufficient to
increase bacterial uptake (2, 3), at least for low–
molecular weight substrates. For example, relatively strong turbulence (D = 10−6 W kg−1, where
D is the turbulent dissipation rate) increases the
uptake of amino acids by <1%, and as a result
turbulence has been considered inconsequential
for bacterial uptake (2).
Many DOM sources occur as small, discrete
patches, including cell lysis, phytoplankton exu-
dation, marine snow particles, oil droplets, and
excretions by larger organisms (4, 5). Numerous
bacterial taxa have evolved the ability to sense
chemical gradients associated with patches and
swim toward more favorable conditions (5–8), a
process called chemotaxis. Chemotaxis can affect
marine biogeochemical cycles by increasing re-
mineralization rates (5, 9), and community com-
position by affording motile bacteria a benefit
over nonmotile competitors (7). Yet, most knowl-
edge of chemotactic foraging is based on studies
in still fluid, simple flows, or synthetic advection
(7, 10, 11).