Rotifers!

 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.

O’Leary, 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/

Weinhold, Bob. 2006. “Epigenetics: the science of change.” Environmental Health Perspectives, 114(3): A160-A167.

Williams, Sarah. 2015. “Humans may harbour more than 100 genes from other organisms”. Science, March 12, 2015. Online: http://www.sciencemag.org/news/2015/03/humans-may-harbor-more-100-genes-other-organisms