New research on the emergence of the first complex cells challenges orthodoxy

August 8, 2022

In the beginning, there was boredom. Following the emergence of cellular life on Earth, some 3.5 billion years ago, simple cells lacking a nucleus and other detailed internal structure dominated the planet. Matters would remain largely unchanged in terms of evolutionary development in these so-called prokaryotic cells — the bacteria and archaea — for another billion and a half years. 

Then, something remarkable and unprecedented took place. A new type of cell, known as a eukaryote, emerged. The eukaryotes would evolve many complex internal modules or organelles, including the endoplasmic reticulum, the Golgi apparatus and the mitochondria, forming wildly diverse cell types — precursors to all subsequent plant and animal life on Earth.  Illustration of a prokaryotic cell and a eukaryotic cell. Prokaryotic cells, which include bacteria and archaea, are structurally simple organisms, lacking the complex internal structure found in eukaryotes. All living plant and animal species today have their origins in the last eukaryotic common ancestor, or LECA. The transition from prokaryote to eukaryote has remained a central mystery biologists are still trying to untangle. Download Full Image

How this crucial transition came to be remains a central mystery in biology. 

In a new study, Paul Schavemaker, a researcher with the Biodesign Center for Mechanisms of Evolution at Arizona State University, and Sergio Muñoz-Gómez, formerly with ASU and currently a researcher with the Université Paris-Saclay, Orsay, France, take a fresh look at the puzzle of eukaryotic emergence.

Their study, which appears in the current issue of the journal Nature Ecology & Evolution, challenges a popular scenario put forward to explain the arrival of the first eukaryotic organisms.

The researchers explore in detail the energy requirements of eukaryotic cells, which are on average larger and more complex compared with prokaryotes. Their quantitative results stand in opposition to a reigning dogma, first put forward by biologists Nick Lane and Bill Martin.

Genesis to revelation

The basic idea of Lane and Martin is that a cell’s developmental fate is governed by its supply of energy. Simple prokaryotes are mostly small and consist of single cells or small colonies, and can subsist on more limited stores of energy to power their activities. But once a cell achieves sufficient size and complexity, it eventually reaches a barrier, beyond which such prokaryotes cannot pass. Or so the theory has it.

According to this idea, a singular event in Earth’s history gave sudden rise to the eukaryotes, which then grew and diversified to occupy every ecological niche on the planet, from undersea vents to arctic tundra. This vast diversification occurred when a free-living prokaryotic cell acquired another tiny organism within the confines of its interior. 

Through a process known as endosymbiosis, the new cell resident is taken up by this proto-eukaryote, supplying it with additional energy and enabling its transformation. The endosymbiont it has acquired would eventually develop into mitochondria — cellular powerhouses found only in eukaryotic cells.

Because all complex life today can be traced to a single eukaryotic branch of the evolutionary tree, it has been assumed that this chance endosymbiotic event, the acquisition of mitochondria, occurred once and only once during the entire history of life on Earth. This accident of nature is why we’re all here. Without mitochondria, the larger volume and complexity of eukaryotes would not be energetically viable.

Not so fast, the authors of the new study claim.

Crossing the borderlands

Portrait of ASU researcher .

Paul Schavemaker

Schavemaker notes that while the distinction between prokaryotes and eukaryotes among organisms living today is obvious, things were murkier during the transition phase. Eventually, all the common traits of extant eukaryotes would be acquired, yielding an organism researchers refer to as LECA, or the last eukaryotic common ancestor.

The new study explores the advent of the first eukaryotes and notes that instead of a hard boundary line separating them from their prokaryotic ancestors, the true picture is messier. Rather than an unbridgeable gulf between prokaryotes and eukaryotes in terms of cell volume internal complexity and number of genes, the two cell forms enjoyed considerable overlap.

The researchers investigate a range of prokaryotic and eukaryotic cell types to determine a) how cell volume in prokaryotes can eventually act to constrain a cell’s membrane surface area required for respiration, b) how much energy a cell must direct to DNA activities based on the arrangement of its genome, and c) the costs and benefits of endosymbionts for cells of various volume.

It turns out that cells can grow to considerable volume and acquire at least some of the characteristics of complex cells while remaining primarily prokaryotic in character and without the presence of mitochondria.

Escalating energy demands

The researchers examined how the respiratory requirements of a cell, measured by the number of ATP synthase molecules available to supply ATP energy for cell growth and maintenance, scale with a cell’s volume. They also describe how energy requirements scale with cell surface area, drawing on data from Lynch and Marinov.

“We actually looked at the surface area of the cell and found that the number of ATP synthases increases faster than the cell membrane does,” Schavemaker says. “This means that at some point of increasing cell size, there will be a volume limit, where the ATP synthases cannot supply enough ATP for the cell to divide at a certain rate.”

Eukaryotes overcome this barrier through additional respiratory surface area provided by internal membrane-bound structures like the mitochondria. 

Intriguingly, this cell volume limit does not occur at the boundary of prokaryotes and eukaryotes, as previous theory would predict. Instead, “it happens at much larger cell volumes, around 103 cubic microns, which encompasses a lot of existing eukaryotes. And that's what has made us think mitochondria probably weren't absolutely necessary. They may have helped, but they weren’t essential for this transition to larger volumes,” Schavemaker says.

Graphic illustration of mitochondria.

Mitochondria are the energy powerhouses in eukaryotic cells. One popular hypothesis claims these organelles were a prerequisite to the transition from simpler prokaryotes like bacteria and archaea to larger, more complex eukaryotic organisms. The new study challenges this assumption. Graphic by Jason Drees

Something similar happens when the arrangement of genes within prokaryotes and eukaryotes is compared. The genome architecture of prokaryotes is said to be symmetrical, consisting of a circular, double-stranded length of DNA. Many bacteria harbor multiple copies of their genome per cell.

But eukaryotes have a different genome architecture, known as asymmetrical. The key advantage of the eukaryotic genome arrangement is that they don't have to maintain genome copies all over the cell, like prokaryotes. For most genes, eukaryotes can maintain one or two copies in the nucleus; only a small number of genes are present on the many copies of the mitochondrial genome that are strewn throughout the cell.

In contrast, large bacteria have many copies of their entire genome, with each genome containing a copy of every gene, present throughout the cell. This distinction has allowed eukaryotes to grow considerably in size without facing the same energy constraints imposed on prokaryotes. But once again, the researchers observed significant overlap in the gene numbers of prokaryotes and eukaryotes, suggesting that prokaryotes can expand their gene number into the domain usually associated with larger eukaryotes, until they reach a critical threshold beyond which their genomic symmetry becomes a limiting factor.

LECA revisited

The new picture of early eukaryote evolution provides a plausible alternative to the mitochondria-first paradigm. Rather than evolution ushering in the age of eukaryotes with one grand gesture — the chance acquisition of a mitochondrial prototype, a series of tentative, gradual, step-wise changes over vast time spans ultimately produced complex cells packed with sophisticated internal structures and capable of explosive diversification. 

Earlier research by Lynch and Marinov cited in the new study takes a somewhat more radical view, implying that mitochondria offered few if any benefits to early eukaryotes. The new study stakes out a more moderate position, suggesting that beyond a critical cell volume, mitochondria and perhaps other features of modern eukaryotic cells would have been necessary to satisfy the energy needs of large cells, but a range of smaller proto-eukaryotes may have done just fine without these innovations.

Hence, the transition to the mysterious LECA event may have been preceded by a series of organisms, which may have initially been mitochondria-free.

The new research also throws into question the timing of eukaryotic transition events. Perhaps the great transition began with the development of a eukaryotic cytoskeleton or other advanced structure. The internal mitochondria with its additional cellular genome may have started when a smaller prokaryote was engulfed by a larger one, through a process known as phagocytosis, or perhaps the mitochondria invaded the first prokaryote as a parasite. Much more research will be required to confidently place the series of events leading to fully fledged eukaryotes in their proper sequence.

“We don't know which advances came first,” Schavemaker says. “You could imagine a series of organisms that first started with endomembranes and internal vesicles. Then, they develop the ER from this, which carries out the handling of the membrane proteins, and from this you get the nucleus. And maybe then the mitochondria came in by phagocytosis. There’s a whole series of steps you can imagine. But where you say, ‘Oh, this is a eukaryote and this is still a prokaryote,’ — you cannot really do that.”

Richard Harth

Science writer, Biodesign Institute at ASU


Breaking new ground

One of few Native American women with an advanced construction degree could help enrich the industry’s cultural landscape

August 8, 2022

Brianne Arviso could have easily stepped into an entry-level job in the construction industry after graduating from high school.

At that time, the Arviso Construction Company, started by her grandfather, Olsen Arviso Sr., had been in business for more than two decades. Her father, uncles and aunts worked for the company, headquartered near Gallup, New Mexico, on the Navajo Nation. professor and student embrace at doctoral degree graduation ceremony Brianne Arviso (right) is a member of the Navajo Nation, originally from Iyanbito, New Mexico. She is Tabaaha (Waters Edge Clan), born from the Kinyaa’aanii (Towering House People). Arviso is pictured at the Ira A. Fulton Schools of Engineering Spring 2022 Convocation ceremony at Arizona State University with her doctoral studies adviser, Associate Professor Kristen Parrish, the construction graduate studies program chair in the Del E. Webb School of Construction. Photo by Erika Gronek/ASU Download Full Image

“I grew up with the company being a big part of my world,” she says.

Still, Arviso remembers feeling the pull of a higher calling. To start with, she wanted to go to college.

“But I didn’t want to go to any schools nearby because I didn’t want to be so close that I would lose focus and motivation and just come back home every night,” Arviso says. “I kind of wanted to get out into the world on my own. I wanted to challenge myself.

She knew Arizona State University was welcoming to Native Americans. For one, it offered in-state tuition to people from the Navajo Nation, even for those from reservation communities not in Arizona.

She also knew the percentage of Native American students graduating from ASU was higher than at many other universities.

Arviso signed up as a business management major, with the idea of seeking a career in leadership positions. But after a year in the program, an academic adviser talked to her about something she had somehow remained unaware of — specifically, the Del E. Webb School of Construction within the School of Sustainable Engineering and the Built Environment, one of the seven Ira A. Fulton Schools of Engineering at ASU.

A few years later, Arviso had both a bachelor’s degree in construction management and on-the-job experience working part time for a few Phoenix-area building contractors.

After graduation, she got a full-time position with a leading construction company in the Southwest, Kitchell Corporation. Around that time, however, Arviso’s grandmother, Ernestine, passed away.

“My job was good,” she says, “but my grandmother was the center of everything in our family, so that made me feel kind of lost and I wasn’t sure what I wanted to do.”

During that period of reflection, Arviso would remember that she had always felt happy being in school and on campus.

Portrait of ASU graduate Brianne Arviso in her cap and gown and traditional Navajo dress.

Along with her commencement regalia for the spring 2022 ceremony celebrating recent graduates of Ira A. Fulton Schools of Engineering doctoral programs, Brianne Arviso wore a Navajo rug dress, called a biil, and traditional turquoise jewelry. The dress was made for Arviso and gifted to her by her friend Craig Spencer and his family. Photo courtesy of Brianne Arviso

“It became a turning point in my life that led me to pursue a master’s degree,” she says.

She returned to ASU to earn a master’s degree and in that program found a supportive environment that helped “fill the void from the loss of my grandmother,” she says.

It was then that she also moved beyond studies and into research, focusing on exploring construction in tribal communities — and finding “there was almost nothing,” she says, in the way of extensive studies of the social issues surrounding construction practices on tribal lands.

Arviso recalls how around that time a former teacher, William Badger, today a Fulton Schools professor emeritus, encouraged her to pursue a doctoral degree.

“He told me, ‘You could be the first Navajo woman with a PhD to teach in the Del E. Webb School of Construction,’” Arviso says.

Arviso graduated this past spring as one of the Fulton Schools’ honored doctoral degree recipients — and more significantly, as one of the very few Native American people to attain such a high level of academic achievement in the construction field.

The School of Sustainable Engineering and the Built Environment has maintained an enrollment of about 30 to 35 Native American students in its degree programs — just under 2.5% of the school’s population over the past five years. That includes about 12 to 14 students consistently enrolled in the construction program.

Four Native American students earned a master’s degree in construction in the past year, and one earned a master’s degree in civil engineering, according to Michael Sever, the assistant director of academic services for the School of Sustainable Engineering and the Built Environment.

Those who have served as mentors and advisers during Arviso’s impressive higher education journey say her achievement is about much more than developing technical and management skills.

“Her accomplishment is inspiring,” says Associate Professor Kristen Parrish, chair of the Fulton Schools construction graduate studies program and Arviso’s doctoral studies adviser. “She is driven and ambitious, and one of the best learners and hardest workers I’ve seen.”

Arviso has demonstrated those qualities in her doctoral work, which has included extensive research on tribal socioeconomic and cultural challenges faced by the construction industry on Native American lands.

By the time she completed her doctoral studies, Arviso “was already on the front lines as a trailblazer” in efforts to bring advances in construction practices to those underserved populations, Parrish says.

Arviso was also proactive in efforts to aid other students, says Professor Emeritus Allan Chasey, a former Del E. Webb School of Construction program chair. He interacted with Arviso in ASU’s Construction in Indian Country, or CIIC, organization, and notes her contributions to recruiting other Native American students.

“She was hard-working and organized, and always available to take on projects and to ensure the end result was a success,” Chasey says. “She was a model student and demonstrated talents and abilities that I think will help ensure her success.”

Marcus Denetdale, the current CIIC program manager, views Arviso as the kind of astute and resilient crusader needed to advocate for Native Americans’ involvement in contributing to the evolution of today’s construction industry.

“Over the past five years, she has been really good about keeping me current on things that are happening in the industry,” Denetdale says. “Brianne has also been promoting disruption in this male-dominated business culture for years. If anyone asks me if there’s someone who can speak about the importance of women in construction, she’s one of the first people I call.”

With Arviso’s achievements to date, Denetdale adds, “She has the potential to be a role model who might inspire other women who are hesitant to get into the field.”

That view of Arviso is shared by architect Wanda Dalla Costa, a faculty member in both the Del E. Webb School of Construction and The Design School at ASU.

Brianne Arviso and father, Olsen Arviso, Jr., Arviso Construction Company

Brianne Arviso poses with her father, Olsen Arviso Jr., at the site of one of the Arviso Construction Company’s recent projects, the Math and Science Building at Diné College in Shiprock, New Mexico. Photo courtesy of Brianne Arviso

A member of the Saddle Lake First Nation, Dalla Costa has for two decades worked with North American Indigenous communities. She founded the Indigenous Design Collaborative and teaches in a service learning studio, both of which enable students to engage with local tribal communities.

“This profession needs more people who come from different circles, who think in different ways, who push back on accepted norms in construction and related industries, and who can potentially open new pathways that move communities forward,” Dalla Costa says.

Because of Arviso’s advanced formal education in the field, along with management and on-the-ground experience gained in work for successful construction companies including her family’s company, Dalla Costa sees Arviso as “a young woman of color who is now in a position to be a very important role model to the next generation.”

Arviso says she has been especially proud of drawing on her own cultural heritage and knowledge in her studies and research at ASU, particularly in her doctoral dissertation.

“Navajos have been developing and applying their own construction planning and design for a very long time. It has just never been documented,” she says.

Her doctoral dissertation focused on pre-project construction planning for tribal communities, but also included a chapter specifically on drawing the connection between the roots of the fundamental philosophy of life of the Diné, the Navajo people, and their approaches to building and improving their communities.

Now, in her work for Arviso Construction’s commercial ventures, she can contribute to planning, budgeting, cost projection, labor management, design and related architectural styling, as well as scheduling and overseeing day-to-day building operations.

Equally as important, she says, is understanding the basic idea of why each project is being built and what the owners want the structures to provide for their businesses and for their communities.

“So, it’s all about really understanding every aspect of construction and all the details,” Arviso says, “but also understanding the people you are building for and their goals and their environment and their outlooks on things.”

While her construction career has been evolving, Arviso also started a flower shop in Gallup, New Mexico, close to the Navajo reservation border. She’s taking on the myriad tasks of operating the small retail business, which has meant learning about providing customer service, managing employees, expenses, inventory, bills and taxes.

Arviso’s entrepreneurial spirit “is one reason I find her so amazing,” says Parrish, her adviser.

“She is the seventh PhD student I’ve advised, and I’m proud of all of them. But she’s the one I’m probably most proud of because her journey was more challenging than for most people,” Parrish says. “She has a real desire to give back to her community. So to see her being successful is really exciting.”

Arviso says she has fulfilled her biggest educational aspiration by being the first Navajo woman to earn bachelor’s, master’s and doctoral degrees from the Del E. Webb School of Construction.

The only way to exceed that achievement, she says, “is to someday have my own Brianne Arviso School of Construction.”

Joe Kullman

Science writer, Ira A. Fulton Schools of Engineering