Moselio Schaechter


  • The purpose of this blog is to share my appreciation for the width and depth of the microbial activities on this planet. I will emphasize the unusual and the unexpected phenomena for which I have a special fascination... (more)

    For the memoirs of my first 21 years of life, click here.

Associate Bloggers



  • (Click photo for more information.)

Bloggers Emeriti


  • (Click photo for more information.)

Meetings & Sponsors



« Prophage Masquerade | Main | The Next Generation (Or Two) »

February 22, 2010

Mother’s Love

by Elio

Hi_bud

Binary fission is a most impressive invention. In one fell swoop, it ensures that progeny cells are born alike and endowed with the same potential for growth and survival. Simple as it sounds, it must have taken considerable evolutionary contortions to make it function so well throughout the living world. But there are cells that have adopted an alternative mechanism, where cell division is asymmetrical, where one progeny cell is made from a “mother cell” that keeps generating “babies.” The best known example is, of course, budding in yeast. But other cells also arise in this fashion, including some bacteria, the sexual spores of mushrooms, and even some plant cells.

Polarisome

The polarisome in a forming yeast bud. Actin cables
growing out from the polarisome transport protein
aggregates to the mother cell. Source.

So, is there an advantage to bypassing binary fission and budding instead? It would seem that way. Recent work from Tom Nyström’s lab has shown that proteins that become damaged in the course of cell growth flow back into the mother cell and leave the young bud free of such impediments. The damage to proteins is often due to oxidation by reactive oxygen species. Damaged proteins tend to form aggregates. This can be bad, getting rid of them is good. How do these proteins accumulate in the mother cell? Interestingly, protein aggregates hitch a ride on actin filaments that grow from the growing bud to the mother cell. Such filaments are assembled at the tip of the bud in a structure the authors call a “polarisome,” which is made up of core proteins plus some involved in actin polymerization (formins). Also required is the age-retardant deacetylase, a protein called Sir2 and aka sirtuin. Previously known as a life span modulator—not just in yeast but in worms, fish, and mammals as well—Sir2 has now been found to also be involved in actin-related processes, hence in polarisome formation. It gets more complicated. For an overview, we suggest a commentary by Guarente.

Mother_cell

(A) Exponentially growing young yeast cells to compare their size and
morphology to that of old cells. (B) A typical lifespan determination.
The number of budding cycles that each of a set of 50 ‘virgin’ cells
undergoes before it stops dividing was determined by micromanipu-
lation and counting of budding cycles. (C) M is the terminal mother cell
after 15 cell cycles. Note the enormous size as compared to young cells
and the surface changes. D14 is the second but last daughter that did
not completely separate from the mother and did not give rise to new
living cells. Source.

Now let’s look at this story in a broader context. It’s not just about shipping dirty laundry off to mother. One consequence of the asymmetry of budding is that the mother cell retains its bodily integrity bud after bud, whereas this is lost when a cell divides by binary fission. In yeast, a mother cell can bud some 15-30 times, after which it conks out. How do we know? Counting the number of times a cell gives off buds is done patiently under the microscope, using a micromanipulator to remove each daughter cell once it separates from the mother cell. Keep this up until the mother cell gives off no more buds. Imagine teasing the new cells away for the mother cell 30 times or so! (This seems to have been done first in 1950 by A. A. Barton, working for a British brewing company.) This phenomenon is called senescence, and is visually illustrated by wrinkles of old age and the unusually large size of the Grande Dame. Newly formed cells start the process anew, each daughter cell becoming a mother cell of its own. However, in time, the newly made cells are less competent for further budding. Not surprisingly, yeast is a favorite for studies of cell polarization and its possible role in senescence. Many papers have been written on this subject.

A favorite connection between yeast budding and aging relies on a 120-year-old theory by August Weismann. He postulated that aging evolved from the need to separate germ cells from somatic cells. Germ cells need to be protected from damage; somatic cells can ”take it.” One of the reasons given is that additional resources must be bestowed on germ cells to ensure their genetic stability. Somatic cells, in contrast, do not have such mechanisms and thus accumulate damage.

This is one way to think about asymmetric cell division. Formally speaking, the mother cell acts as a somatic cell that produces multiple germ cells, the buds. Each, when grown, becomes a mother cell with full reproductive potential, able to produce a full complement of buds of her own. During budding, the young bud escapes from the cell damage represented by the aggregated proteins, thus foiling at least that aspect of cell aging.

If asymmetric cell division affords such protection of the germ line, why don't all cells do this? The question is not terribly relevant to multicellular somatic cells, given that they are not involved in germ line propagation (unless some investigator teases their nuclei out and introduces them into eggs). But how come more unicellular microbes haven't adopted the budding strategy? That is a question for another time.

Given that yeast is the best known of all eukaryotic organisms, allowing endless kinds of genetic manipulations, it’s no wonder that it has become a model for the study of aging. And here I thought that I would be a good subject for researching what happens in old age!

Addendum: As Qetzal noted (see his comment below), I could have mentioned that a possibly analogous phenomenon has been reported for bacteria. When E. coli divides, the "old" cell pole accumulates chaperones involved in the aggregation of (presumably) damaged proteins. Eventually the "old" cells lose their reproductive capability. Something analogous takes place in Caulobacter crescentus. Thus, bacteria may also use the strategy of segregating damaged proteins in aging cells, to the advantage of the population as a whole.

ResearchBlogging.org

Liu, B., Larsson, L., Caballero, A., Hao, X., Öling, D., Grantham, J., & Nyström, T. (2010). The Polarisome Is Required for Segregation and Retrograde Transport of Protein Aggregates Cell, 140 (2), 257-267 DOI: 10.1016/j.cell.2009.12.031

Comments

It can be added that, among prokaryotes budding also serves a disbursal function. Caulobacter was mentioned and Hyphomonas is another, perhaps more interesting, example. The mother cell actually "flings" its progeny buds away, freeing them to seek more fertile niches on aquatic substrata. The following is a "classical" article which
provides more information.

PM Zerfas, M Kessel, EJ Quintero, et al.
1997. Fine-structure evidence for cell membrane partitioning of the nucleoid and cytoplasm during bud formation in Hyphomonas species. J. Bacteriol. 179(1):148-156.

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC178673/

Yuri,

What sharp questions you ask. Surely someone has the answers, at least in part. They would be most welcome in this blog.

Interesting comment. What details are known about the distribution and metabolic activity of mitochondria in budding yeast? Bursts in biosynthesis must be accompanied by accelerated respiration. I would assume this is the source of oxidative stress. Are mitochondria that partition to the bud genetically and metabolically identical to those that remain with the mother cell?

I'm struck by the similarities between this and the recent discoveries about aging in bacteria. Even though the products of binary fission appear identical, age appears to be 'inherited' via the cell poles. (You posted about those in Oct 2007 - http://schaechter.asmblog.org/schaechter/2007/10/do-bacteria-age.html).

Isn't there even some similar evidence about sequestering damaged proteins with the older pole in bacteria? I can't remember clearly, and couldn't find it after a quick search.

Verify your Comment

Previewing your Comment

This is only a preview. Your comment has not yet been posted.

Working...
Your comment could not be posted. Error type:
Your comment has been saved. Comments are moderated and will not appear until approved by the author. Post another comment

The letters and numbers you entered did not match the image. Please try again.

As a final step before posting your comment, enter the letters and numbers you see in the image below. This prevents automated programs from posting comments.

Having trouble reading this image? View an alternate.

Working...

Post a comment

Comments are moderated, and will not appear until the author has approved them.

Teachers' Corner

Podcast

How to Interact with This Blog

  • We welcome readers to answer queries and comment on our musings. To leave a comment or view others, remarks, click the "Comments" link in red following each blog post. We also occasionally publish guest blog posts from microbiologists, students, and others with a relevant story to share. If you are interested in authoring an article, please email us at elios179 at gmail dot com.

Subscribe via email

Translate




Search




MicrobeWorld News

Membership