permaculture

[Lawrence London <lfljvenaura@gmail.com>]

Microscopic menagerie | Science News - New view of microbes forces
rethinking of what it means to be an organism
https://www.sciencenews.org/article/microscopic-menagerie?utm_source=Society+for+Science+Newsletters&utm_campaign=2b3885385c-Editor_s_picks_week_of_December_22_2014_12_24_2014&utm_medium=email&utm_term=0_a4c415a67f-2b3885385c-104492597

Feature
 Microbes <https://www.sciencenews.org/search?tt=79>,
Microbiology <https://www.sciencenews.org/search?tt=93>
 Microscopic menagerie
 New view of microbes forces rethinking of what it means to be an organism
  By
  Susan Milius <https://www.sciencenews.org/author/susan-milius>
   2:05pm, December 27, 2013

*MADE OF MICROBES*  The microbes dwelling in and on multicellular
organisms, such as insects and humans, should be viewed as evolutionarily
inseparable from their hosts, some biologists argue.

Nicolle Rager Fuller
  Magazine issue: Vol. 185 No. 1, January 11, 2014
<https://www.sciencenews.org/sn-magazine/january-11-2014>

What is a wasp?” might seem like an overly simple question for a Ph.D.
biologist to be asking. “What is a human?” Even more so.

But these are strange times in the life sciences. Seth Bordenstein of
Vanderbilt University in Nashville now embraces the notion that each wasp
he studies, each squirrel darting around campus — not to mention himself,
every reader of science magazines and every other representative of
see-it-without-a-microscope life on Earth — is really a blend of one big
organism and a lot of little ones.

In recent years, research has shown that what people commonly think of as
“their” bodies contain roughly 10 microbial cells for each genetically
human one. The microbial mass in and on a person may amount to just a few
pounds, but in terms of genetic diversity these fellow travelers overwhelm
their hosts, with 400 genes for every human one. And a decent share of the
metabolites sluicing through human veins originates from some microbe. By
these measures, humanity *is* microbial.

But numbers are just the beginning.

*GUT BUSTER* Tsetse flies must be infected during gestation with a
particular bacterium in order to develop a normal gut lining (top).
Lab-raised larvae that were bacteria-free developed faulty guts (bottom)
and weak immune systems that made them much more vulnerable to infection by
the parasite that causes sleeping sickness.
Weiss *et al/PLOS Pathogens* 2013
The evolutionary impact of animals’ microbial denizens can be substantial.
Adult wasps of the genus *Nasonia* are only about 30 percent microbial,
Bordenstein estimates. But those microbes keep two species apart that could
otherwise interbreed.

Some researchers think of these microbes as just another part of a plant or
animal’s environment, like a mountain range that keeps two related species
separate. But, with a squint and a slap to the worldview, researchers like
Bordenstein are exploring whether a body’s microbes are so intimate that
they’re part of the organism itself. Or, if you prefer, the metaorganism.

“Ecosystem” is the word that 26 scientists used in a call for new thinking
about animal-bacteria interactions that was published in February by
the *Proceedings
of the National Academy of Sciences*. The recent accumulation of knowledge
about bacteria vis à vis their animal hosts “is fundamentally altering our
understanding of animal biology,” the group declared.

Why would biologists get so excited about teeming microorganisms now? Even
someone who missed the earliest fiddling with magnifying lenses has had 330
years to catch up on volume 14 of the Royal Society’s *Philosophical
Transactions*, wherein merchant microscopist Antonie van Leeuwenhoek
reported “to my great surprise,” that watered-down scrapings from his teeth
revealed “very many small living Animals, which moved themselves very
extravagantly.”

For more than three centuries after van Leeuwenhoek’s discovery, anyone
interested in studying the microbial world was limited by the frustrations
of “growing fuzzy things in Petri dishes,” as Corrie Moreau of the Field
Museum in Chicago puts it. A fascinating microorganism might thrive in the
gills of deep-ocean clams, in groundwater seeping through porous rock or in
the gonads of mosquitoes. But if you couldn’t culture it in a lab dish you
had no way of knowing about it. Even with clever technical advances, an
estimated 99 percent of microbial life can’t be cultured, Moreau says. And
what does grow may be misleading. A marginal freak may look like the
dominant member of a community only because it’s the one that flourishes in
the lab.

Recent genomic innovations have changed all that. In the last few years,
automated systems have been developed to quickly and affordably determine
the genetic signatures of thousands of individual microbes in a sample.

What a world the new technology reveals: In just 19 samples from four
colonies of turtle ants, Moreau says, 445 kinds of bacteria showed up that
cultures and clunkier genetic techniques had missed. Eight kinds of
bacteria consistently show up in the guts of honeybees and a few other
bees, but so far, nowhere else. Bedbugs need *Wolbachia* bacteria inside
their cells to survive.

And bacteria may at last explain how the giant panda, a bamboo-eating
member of the mammalian order Carnivora without a grass-grazer’s capacious
fermenting gut or specialist digestive enzymes, can live on 12.5 kilograms
of highly fibrous plant material a day. The bear’s puzzling digestive
system turns out to gurgle with bacteria that apparently belong to groups
that include competent digesters of cellulose.
*Born with it*

Bacteria start shaping their hosts’ lives right from the beginning. In
tsetse flies, for example, inheriting genes from mom isn’t enough; larvae
that don’t also inherit the right kind of bacteria don’t grow properly.

The way tsetse flies start their lives “is eerily similar to what happens
in mammals,” says Brian L. Weiss of Yale University. In most insects, “the
female will just lay a bunch of eggs and fly away.” Tsetse females,
however, gestate one fertilized egg at a time inside what amounts to a
uterus. Glands inside the uterus produce a white milklike liquid rich in
fats and proteins. After suckling for its first three larval stages, the
youngster weighs about as much as its mother. Then she gives birth.

Gorging on mother’s milk doses the infant with a *Wigglesworthia*
bacterium, which Weiss describes as looking like a hot dog. *Wigglesworthia*
can live only inside a tsetse fly, and flies deprived of it don’t give
birth.

Weiss was able to deduce what *Wigglesworthia* does in development by
dosing moms with B vitamins to artificially keep their bacteria-free larvae
alive. The larvae grew up but never formed a decent immune system. Flies
deprived of bacteria as larvae also failed to form a real gut lining, Weiss
and his colleagues reported in April in *PLOS Pathogens*.

A faulty gut lining in a tsetse fly is a serious problem, and not just for
the flies. Even though they’re famous for spreading the trypanosome
parasite that causes sleeping sickness, only 1 to 5 percent of normal
tsetse flies become carriers when feeding on infected blood. With faulty
guts, though, more than 50 percent of bacterially starved, skimpy-gut flies
turn into carriers.

Other studies have turned up similar examples of microbial power in animal
development. Females of the parasitic wasp *Asobara tabida* need a
*Wolbachia* bacterial strain in order to form wasp eggs. Developing mice
can’t form normal capillaries in their guts without a standard set of
microbes being present. And young lab mice may even need their gut bacteria
for proper brain development, a research team in Sweden reported in 2011.
Mice raised without normal gut microbes were unusually active and bold in
tests, as if their brains weren’t wired the same way as those of regular
shadow-loving, skittish mice. Returning gut bacteria to germfree mice
re-created normal caution in their offspring. But it failed in adults with
brains that were already mature.

Moms of a variety of species appear to microbially prep their young, says
Bordenstein. Vesicomyid clams that need microbial help to survive at
deep-sea vents, some sponges and cockroaches release eggs already loaded
with bacteria. When stinkbugs lay eggs, the capsules get smeared with mom’s
bacteria-rich excrement. When the youngsters hatch, they gobble the egg
case, smear and all.

Reports of mother-to-child bacterial transmission appear to be so
widespread among animals, Bordenstein argues, that it’s time to consider
them the norm. He and Vanderbilt colleague Lisa Funkhouser published a
manifesto in August in *PLOS Biology* calling for an end to “the
sterile-womb paradigm.”
*Bacterial billboards*

Other paradigms are drawing strength from microbiologists’ recently
developed ability to genetically probe bacterial communities. Since the
mid-1970s, biologists have suspected that in many mammals a microbial
community ferments various sweats, oozes and excretions into distinctive
scents that reveal age, health and much more to knowing noses in a select
social circle.

The notion sounds plausible, but attempts to test it have stalled for
years. Culturing bacteria from various mammal scent glands has generally
yielded only one or two, or sometimes five, kinds. This paltry haul seemed
too limited to convey all the information that biologists think is wafting
around.

With modern genetic tools to identify bacteria, Kevin Theis of Michigan
State University in East Lansing and his colleagues are revisiting the
classic hypothesis of messaging by fermentation. His scent-marking research
subjects are spotted and striped hyenas.
*Say it with scent Striped and spotted hyenas (shown, top) both use a
smelly paste exuded from pouches under their tails to mark territory and
communicate with one another. A two-dimensional statistical plot showing
variation among bacterial communities hosted by individual hyenas of the
two species (bottom left) looks very much like one showing variation in
chemical components of their scents (bottom right). Sam DCruz/ShutterStock;
K. Theis et al/PNAS 2013 *

“Pretty robust,” is how Theis rates the funk wafting off hyena scent marks.
Both species evert a pouch just under the tail and dab a pungent paste
produced by sebaceous glands onto a grass stem or other convenient
landmark. The paste smells to Theis like pine mulch fermenting after a
rain. It could encode territorial information as well as olfactory gossip
such as who’s growing eager for a mate, already pregnant or perhaps ill.

Hyenas have a lot to smear and sniff about. Spotted hyenas live in
hierarchical clans of dozens of animals. “It’s like watching a soap opera,”
says Theis. Striped hyenas spend more time alone and form smaller groups,
but still need to keep up with their kind while they forage, rest and
travel.

So far, Theis says, he’s found more bacterial genera just in the scent
paste of adult female spotted hyenas than researchers had discovered in 15
earlier studies of any mammalian scent gland.

The blends of stinky volatile compounds that striped and spotted hyenas use
to communicate are distinct enough that biologists can distinguish the two
species by their scent marks. And, as would be predicted if microbes were
making the scents, the two species likewise have distinctive microbial
communities that align with those scent differences, Theis and his
colleagues report November 11 in the *Proceedings of the National Academy
of Sciences*. The link between odor difference and community difference
supports a main pillar of the hypothesis that the microbes are the message.

The researchers also detected some patterns within species suggesting that
the communities shifted with events such as pregnancy. This paper marks the
closest anyone has come to demonstrating the whole fermented-message idea,
Theis says.
*Choice microbes*

Microbial residents do more than broadcast scented status updates. Bacteria
also appear to steer their hosts away from some mates.

One startling example, described in 2010, grew out of a peculiar side
effect of rearing fruit flies on different diets. In earlier experiments,
researchers had noticed that lineages of fruit flies fed for 25 generations
on different diets became less likely to mate with each other.

Follow-up tests at Tel Aviv University found that *Drosophila
melanogaster *flies
rejected opposite-diet flies as potential mates after just one generation
of eating molasses rather than starch. At Tel Aviv, Eugene Rosenberg and
Ilana Zilber­Rosenberg had been formulating ideas on the importance of what
they called the holo­genome, the sum of genetic information in a host
species and its microbial residents. To test this comprehensive view of the
fruit fly, researchers fed the flies antibiotics to kill the insects’
microbial communities. Without microbial influence, the lineages took to
mating with each other again.

Inoculating reconciled fly lineages with different microbial communities
resurrected the mating barrier. What made the difference, researchers
proposed, were diet-based shifts in gut microbes that in turn influenced
sex pheromones.

*A breed apart* When two related species of Nasonia wasp mate (left), their
hybrid male offspring (g/v and v/g) usually don’t survive. With a dose of
antibiotics, however, hybrid males are almost as viable as nonhybrids
(right).
R. Brucker and S. Bordenstein/Science 2013

Observing a microbial effect on mate choice makes it sensible to ask a very
big question: Could these teeming microscopic masses control the
evolutionary fate of whole species?

In jewel wasps, for example, a genetic barrier that keeps two species apart
turns out to have a previously overlooked microbial aspect (*SN: 8/10/13,
p. 13*)
<https://www.sciencenews.org/article/gut-microbes-may-put-barrier-between-species>,
Bordenstein and Vanderbilt colleague Robert Brucker reported in the Aug. 9
*Science*.

Two kinds of jewel wasp, *Nasonia giraulti* and *Nasonia vitripennis*,
split off from a common ancestor about a million years ago. If the two
species happen to mate now, the second-generation male larvae develop a
dark splotch and die. Geneticists have traced this lethal incompatibility
in detail, finding genetic differences between the species that appear to
influence hybrid survival.

To test for a possible missing microbial something, Brucker dosed doomed
hybrids with an antibiotic. Their resident microbes died, but many of the
hybrid wasps lived. A mismatch between their parents’ differing microbes
and their genes seemed to be killing hybrids.

As a further test, Brucker gave the unexpectedly alive germfree hybrids
some of the gut bacteria that hybrids normally have. No longer germ-free,
the hybrids died.

The experiment supports Bordenstein’s view that evolutionary forces act not
just on an animal’s DNA but on the sum of its own genome and those of its
microbial residents.

Microbial incompatibility appears to render hybrid male wasp larvae of two
Nasonia species much less viable than purebreds.
R. Brucker and S. Bordenstein/*Science* 2013

Of course microbes matter, says Tadashi Fukami of Stanford University. But
he isn’t ready to declare them and their hosts a single evolutionary
entity. He studies the microbial communities living in flowers’ nectar, and
applauds increased attention to microbial influences. Yet he says that he
would expect the hologenome theory of evolution to apply only in
specialized, albeit interesting, cases. The discussion reminds him of
debates over what’s called group selection. The idea that evolution acts on
groups of organisms caused excitement and controversy when first proposed.
But now Fukami and a fair number of other evolutionary biologists don’t
find many cases in which it applies.

Still, appreciating microbes’ evolutionary significance could upend some
fundamental ideas taught in introductory biology, says developmental
biologist Scott Gilbert of Swarthmore College in Pennsylvania. Learning
that a normal set of mouse genes isn’t sufficient to grow a healthy mouse
body “set off all kinds of gongs and whistles,” he remembers. “All this
stuff about ‘you are who you are depending on your nuclear genes’ was
demonstrably not true,” he says, if microbes living symbiotically in the
body amount to a second mode of inheritance.

He’s embracing the idea of animals as composite beings. On occasion he
finishes scientific presentations with a closing PowerPoint slide that
credits the talk not to him alone, but to “Team Scott Gilbert.”
Citations

M. McFall-Ngai et al. Animals in a bacterial world, a new imperative for
the life sciences <http://www.ncbi.nlm.nih.gov/pubmed/23391737>. *Proceedings
of the National Academy of Sciences*. Vol. 110, February 26, 2013,
p. 3229-36. doi: 10.1073/pnas.1218525110.
B. Weiss et al. Trypanosome Infection Establishment in the Tsetse Fly Gut
Is Influenced by Microbiome-Regulated Host Immune Barriers
<http://www.plospathogens.org/article/info%3Adoi%2F10.1371%2Fjournal.ppat.1003318>
.* PLoS Pathog.* Vol. 9, April 18, 2013, p. e1003318.
doi:10.1371/journal.ppat.1003318.

K. Theis. Symbiotic bacteria appear to mediate hyena social odors
<http://www.pnas.org/content/110/49/19832>. *Proceedings of the National
Academy of Sciences*. Vol 110, December 3, 2013, p. 19832.
doi: 10.1073/pnas.1306477110.
  Further Reading

S. Milius. Microbes help hyenas send status updates
<https://www.sciencenews.org/blog/science-ticker/microbes-help-hyenas-send-status-updates>.
Science News Online. November 11, 2013.

S. Milius. Gut microbes may put barrier between species
<https://www.sciencenews.org/article/gut-microbes-may-put-barrier-between-species>
. *Science News*. Vol. 184, August 10, 2013, p. 13.