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Asymmetry and inequity in the inheritance of a bacterial adhesive

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Asymmetry and inequity in the inheritance of a bacterial adhesive
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Abstract
Pseudomonas aeruginosa is an opportunistic human pathogen that forms biofilm infections in a wide variety of contexts. Biofilms initiate when bacteria attach to a surface, which triggers changes in gene expression leading to the biofilm phenotype. We have previously shown, for the P. aeruginosa lab strain PAO1, that the self-produced polymer Psl is the most dominant adhesive for attachment to the surface but that another self-produced polymer, Pel, controls the geometry of attachment of these rod-shaped bacteria—strains that make Psl but not Pel are permanently attached to the surface but adhere at only one end (tilting up off the surface), whereas wild-type bacteria that make both Psl and Pel are permanently attached and lie down flat with very little or no tilting (Cooley et al 2013 Soft Matter 9 3871–6). Here we show that the change in attachment geometry reflects a change in the distribution of Psl on the bacterial cell surface. Bacteria that make Psl and Pel have Psl evenly coating the surface, whereas bacteria that make only Psl have Psl concentrated at only one end. We show that Psl can act as an inheritable, epigenetic factor. Rod-shaped P. aeruginosa grows lengthwise and divides across the middle. We find that asymmetry in the distribution of Psl on a parent cell is reflected in asymmetry between siblings in their attachment to the surface. Thus, Pel not only promotes P. aeruginosa lying down flat on the surface, it also helps to homogenize the distribution of Psl within a bacterial population.
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Computeranimation
Transkript: Englisch(automatisch erzeugt)
Biofilms are communities of interacting bacteria that are bound to each other and often to a solid surface by a matrix of polymers that the bacteria produce.
In biofilms, bacteria resist antibiotic treatment and the immune system, and they cause infections in tissues and on medical devices that can often only be cured by transplant amputation or surgery to remove the device. Biofilms start when single cells attach to a surface
stuck down by the same types of polymers that will later be important components of the matrix. Then the bacteria divide and proliferate so that the surface-bound population increases. Attachment to a surface also signals bacteria to change the way their genes are expressed to make the transition from the free-swimming state,
called the planktonic state, to the biofilm state. Here we look at an important human pathogen named Pseudomonas aeruginosa to find out how this bacterium controls the distribution of sticky polymer on the surfaces of single bacterial cells and how the inheritance of sticky polymer propagates
from parent cells to daughter cells. In work we published in the journal Soft Matter in 2013, we showed that bacteria that make two types of polymers, named PSL and PEL, spend almost all their time lying flat on a surface. Bacteria that make only one type of polymer, PSL, spend a lot of time attached to only one end,
so they're tilting up off the surface at an angle. Here we show that bacteria that make only PSL tend to have PSL concentrated at one of their ends, but bacteria that make both PSL and PEL tend to have PSL distributed more evenly over their rod-shaped bodies. Because PSL is very sticky to the surface,
these bacteria will be much more sticky at the end with PSL and less sticky at the other end. This is probably the reason these bacteria spend a lot of time tilting up off the surface, attached to their one sticky end. These bacteria proliferate by growing longer and longer and then dividing across the middle. So if a parent cell has an uneven distribution
of sticky polymer along its surface, its daughter should inherit different amounts of sticky polymer coating their surfaces. That's the inequity in our title. We see this type of epigenetic inheritance for both daughters and granddaughters. A cell is more likely to tip up off the surface if it inherited less sticky polymer
from its parent and grandparent. And it's more likely to lie down flat on the surface, strongly attached, if it inherited more sticky polymer. More broadly and speculatively, our results suggest that evolution may have acted to regulate symmetry, both of how bacteria attach to the surface and how the sticky PSL polymer is inherited
as a population propagates. If so, this suggests that symmetry is important and adaptive for this species of bacterium. One possible reason why might be that tighter coupling to the surface helps the bacteria sense the surface more strongly and make a better transition
from the free-swimming planktonic state with its associated patterns of gene expression to the biofilm state, which has very different patterns of gene expression. Questions of symmetry and symmetry breaking are pervasive themes in fundamental physics. For example, why is there more matter than anti-matter in the universe? Why is the matter distributed lumpily in the universe
to give us stars and planets and galaxies? But symmetry is much more rarely seen as a theme in biological physics. Our study illustrates a case of biophysical symmetry and symmetry breaking for bacterial cells and shows how physical concepts of symmetry breaking can give new insight into bacterial biology.