How the Bdelloid Rotifer Lived for
Millennia—Without Sex
by Nina Munteanu
As
a child, I always wanted a microscope.
I
would have collected slimy waters from the scum ponds and murky
puddles near my house. I would have brought them home and exposed
them to the light of my microscope. I would then have peered deep
into a secret world, where shady characters and alien forms lurked
and traded.
It
would be many years, when I was in college, before I finally
witnessed this world—so alien, it might have inspired the science
fiction books I wrote later as an adult. As it turned out, I was led
to pursue a Masters of Science degree, studying periphyton
(microscopic aquatic communities attached and associated with
surfaces like rocks and plants) in local streams in the Eastern
Townships of Quebec.
While
my work focused on how diatoms (glass-walled algae) colonized
surfaces, micro-invertebrates kept vying for my attention. Water
fleas (cladocerans), copepods, rotifers, seed shrimps (ostracods) and
water bears sang across my field of vision. They flitted, lumbered,
wheeled and meandered their way like tourists lost in Paris. But this
wasn’t Paris; I’d taken the blue pill and entered the rabbit hole
into another world...
The
Secret—and Dangerous—World of Micro-Organisms
Small
freshwater habitats are home to a highly productive and diverse
collection of micro-invertebrates—multicellular animals that can
barely be seen with the naked eye. Many average from 0.5 to 1 mm in
size and resemble little white blobs; however, a scholar can
distinguish each invertebrate by its unique movement. For instance,
when presented with a jar of pond water, I can usually distinguish
among the wheel-like wandering of a gastrotrich, dirigible-like
gliding of an ostracod (seed shrimp), the vertical goldfinch-style
“hopping” of the cladoceran (water flea) as it beats its
antennae, or the halting-jerking movements of copepods (oar-feet) as
their antennae drive them along like a dingy propelled by an amateur
oarsman.
Alas,
puddles, ephemeral ponds and vernal pools pose sketchy habitats,
given their tendency to appear and disappear. These environments are
ever-changing, unstable, chaotic and unpredictable. Yet, anyone who
has studied these ecosystems understands that they team with life.
When
a puddle or ephemeral pond dries up then reappears with rain, how can
these communities thrive? Do they all die off and then somehow
recruit when the pond reappears? Many of these invertebrates have
evolved creative ways to survive in very unstable environments. Some
form a resting stage—a spore, resting egg or ‘tun’—that goes
dormant and rides out the bad weather.
Animalcules
& Sleeping Rotifers
Rotifers are
cosmopolitan detrivores (they eat detritus) and contribute to the
decomposition of organic matter. Rotifers create a vortex with
ciliated tufts on their heads that resemble spinning wheels, sweeping
food into their mouths. They often anchor to larger debris while they
feed or inch, worm-like, along substrates. Some are sessile
(attached), living inside tubes or gelatinous holdfasts and may even
be colonial. Others move about and may temporarily anchor themselves
as they feed. Rotifers include species that alternate sexual
reproduction with asexual reproduction, depending on environmental
conditions.
|
Bdelloid Rotifer as photographed by Bob Blaylock
|
In
1701, Antonie van Leeuwenhoek observed that “animalcules” (likely
the bdelloid rotifer Philodina
roseaola)
survived drying up and were “resurrected” when water was added to
them. He’d discovered a highly resistant dormant state of an
aquatic invertebrate to desiccation.
Dormancy
is a common strategy of organisms that live in harsh and unstable
environments and has been documented in crustaceans, rotifers,
tardigrades, phytoplankton and ciliates. “Dormant forms of some
planktonic invertebrates are among the most highly resistant …
stages in the whole animal kingdom,” writes Jacek Radzikowski in a
2013 review in the Journal
of Plankton Research.
Radzikowski describes two states of dormancy: diapause
and quiescence.
Diapausing results
in the production of a dormant egg or cyst whose thick envelope or
shell protects it from drying, freezing, mechanical damage, microbial
invasion and predation, UV radiation and harmful chemicals. Many
survive being eaten and can resist vertebrate digestive enzymes,
helping them disperse and colonize isolated water bodies. Diapause is
controlled by an internal mechanism that is initiated by various
cues, such as temperature or photoperiod. In short-lived organisms,
it is typically initiated only in a single ontogenetic stage.
“Breaking of diapause requires specific cues, and not necessarily
the return of favorable conditions,” writes Radzikowski.
Quiescent
dormancy does
not involve the production of a dormant egg or cyst; rather it
involves a transformation of the organism itself into a dormant state
through a process called cryptobiosis. “Quiescence is … induced
directly by the occurrence of harsh environmental conditions. A
quiescent organism can enter this state in many stages of its life,
and remains dormant only until the adverse conditions end,” writes
Radzikowski.
The
All-Female Bdelloid Rotifer
I
recently had a chance to study a pond sample in a Petri dish through
a friend’s microscope. Attached to a pile of detritus shivering in
the current like trees in a gale, were several microscopic rotifers;
they were feeding. Their ciliated disk-like mouths twirled madly,
capturing plankton to eat. Watching them reminded me of my early
research days at Concordia University in Montreal. Probably Philodina
(a bdelloid); I had seen many during my stream research in Quebec.
The
bdelloid rotifer has dispensed with sexual reproduction entirely and
reproduces exclusively by female parthenogenesis. All-female bdelloid
rotifers have thrived for forty
million years. They’re everywhere, in temporary ponds, moss, even
tree bark. Part of the reason for their incredible success lies in
their strategy of quiescent dormancy.
In
response to unfavourable conditions like a pond drying up, bdelloid
rotifers
enter a process called anhydrobiosis,
contracting into an inert form and losing most of their body water.
The bdelloid withdraws her head and foot and contracts her body into
a compact shape called a tun;
a dormant state that remains permeable to gases and liquids. In this
state, bdelloid rotifers can resist ionizing radiation because they
can repair DNA double-strand breaks. Early research noted that
dormant animals could withstand freezing and thawing from −40°C to
100°C and storage under vacuum. They also tolerated high doses of UV
and X radiation. Later work reported that some rotifers could survive
extreme abiotic conditions, such as exposure to liquid nitrogen
(−196°C) for several weeks or liquid helium (−269°C) for
several hours. Dried up adult bdelloid rotifers apparently survived
minus 80°C conditions for more than 6 years.
Dormancy
is an elegant technique to ride out harsh conditions. The bdelloids
can go dormant quickly in any stage of their life cycle—embryo,
juvenile or adult—and they’re capable of remaining dormant for
decades. They can recover from their dormancy state within hours when
the right conditions return and go on reproducing without the need to
find a mate.
Research
has shown that bdelloid mothers that go through desiccation produce
daughters with increased fitness and longevity. In fact, if
desiccation doesn’t occur over several generations, the rotifers
lose their fitness. They need the unpredictable environment to keep
robust. This is partly because they incorporate genes from their
environment during anhydrobiosis. When dormant, they acquire
mobile
DNA
and stitch it into themselves through a process called horizontal
gene transfer (HGT).
Bdelloid
rotifers carry change inside them, through phenotypic plasticity,
physiological stress response mechanisms, or life history
adaptations. That’s why the bdelloid rotifers survived for
millennia and will continue for many more. They are able to keep up
with rapid and catastrophic environmental change, not to mention
something as gigantic as climate change. They adapt by counting on
change.
References:
Munteanu,
Nina. 2020. “A Diary in the Age of Water.” Inanna Publications,
Toronto. 300pp.
Munteanu,
Nina. 2016. “Water Is…The Meaning of Water.” Pixl Press,
Vancouver. 586pp.
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Denise. 2015. “Horizontal gene transfer: Sorry, Darwin, it’s not
your evolution anymore.” Evolution
News,
August 13, 2015. Online:
https://www.evolutionnews.org/201508/horizontal_gene/
Ricci,
C. And D. Fontaneto. 2017. “The importance of being a bdelloid:
Ecological and evolutionary consequences of dormancy.” Italian
Journal of
Zoology,
76:3, 240-249.
Robinson,
Kelly and Julie Dunning. 2016. “Bacteria and humans have been
swapping DNA for millennia”. The
Scientist Magazine,
October 1, 2016. Online:
https://www.the-scientist.com/?articles.view/articleNo/47125/title/Bacteria-and-Humans-Have-Been-Swapping-DNA-for-Millennia/
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Bob. 2006. “Epigenetics: the science of change.” Environmental
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114(3): A160-A167.
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Sarah. 2015. “Humans may harbour more than 100 genes from other
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