Feature: Jill Banfield, extremophile

This feature appeared in the May/June 2012 issue of Australian Life Scientist. To subscribe to the magazine, go here.

Jill Banfield describes herself simply as an ‘earth scientist,’ but that hardly does justice to the sheer breadth of her research interests. She’s as likely to be studying the behaviour of microorganisms in wild environments, or pondering the contingencies of astrobiology, as digging in the earth to see what lurks beneath the surface.

However, Banfield doesn’t see these as disparate disciplines. Rather, she sees them as different ways of studying the same complex biological systems and how they interact with the environment around them.

“My main focus is understanding how microorganisms impact both biological and geochemical processes, including carbon, nutrients and contaminant cycling. I also study how the microbes themselves adapt to environmental challenges and opportunities, as well as ecological processes such as colonisation. The approaches and basic questions cut across ecosystems,” she says.

This is because you can’t properly study life without looking at the environment in which it exists and evolved. “Microorganisms exert fundamental controls on the chemistry of their environments, with their activities shaped by inter-organism interactions and the geochemistry of their surroundings.”

Banfield’s favourite sites for studying such microbial interactions and communities lie literally just below the surface, such as an acid mine drainage system in California, in aquifer sediment in Colorado, in a hypersaline lake in outback Australia and the premature infant gut.

Roots

Banfield was born in Armidale in northern New South Wales, and did her undergraduate degree at the Australian National University in Canberra. She then worked for Western Mining Corporation, a nickel and copper mining company, for a year before realising that the path she was taking was not the right one for her. So she went about rectifying that immediately.

“I returned to ANU and completed my MSc degree on granite weathering, which sparked my interest in the roles microorganisms play in converting rock to soil.” This, in turn, led to a PhD in Earth and Planetary Sciences at Johns Hopkins University in Baltimore in the US, which focused on questions relevant to deeper in the earth.

However, Banfield’s long-term fascination was with near-surface processes, and she soon embarked on a new research direction at the University of Wisconsin, Madison working on the microbial colonisation of rock surfaces by lichens.

“After some twists and turns, I was eventually drawn into the study of microbial communities with modern ‘omics methods. However, I maintain an interest in minerals, primarily the nanoscale ones, such as nanoparticles, made by microorganisms under specific circumstances.”

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Nanoparticles can occur naturally as important components of geochemical cycles in soils, groundwater, rivers and lakes. They may also be introduced into the environment by human activity, either undesirable, as in the case of mining activity and other industrial contamination, or intentional, such as the idea of using engineered nanoparticles for cleaning up contaminated sites.

Since 2001, Banfield has been based at University of California Berkeley, where she is a professor of earth and planetary science, of environmental science, policy and management, and of materials science and engineering, as well as a faculty scientist at Lawrence Berkeley National Laboratory.

Of the many projects she has on the go, Banfield will speak about a select range in her presentation at the Australian Society for Microbiology meeting in July. “Inevitably, it will be what is most exciting to me the week of the meeting. Right now, science is moving so fast I can hardly know!”

That said, it’s safe to predict Banfield’s topic will be either something to do with biofilms or bioremediation, although the human microbiome has an outside running chance, as does carbon cycling in subsurface sediment.

Acid junkies

Another old interest of Banfield’s relates to her extensive research with acid mine drainage. “For many years, my research group and collaborators have been investigating microbial biofilms that develop in highly acidic, metal-rich solutions that we in the USA describe as acid mine drainage,” she says.

Banfield’s group has developed these biofilms as highly useful model systems for studying natural microbial communities. They’ve proven useful in addressing a range of questions surrounding virus-host interaction dynamics and adaptation to extreme environments, to evolution within systems in the face of human-induced perturbation and to just how these communities assemble.

Microbial systems are inherently complex and dynamic, but domination by a handful of organisms in these harsh and very specific biofilm environments makes it possible to thoroughly describe the main populations in terms of their genomic potential and activity.

Applying genomics-enabled methods to such extreme systems with reduced species richness has further boosted a relatively comprehensive understanding of the metabolic networks and evolutionary processes within these communities.

Indeed, Banfield’s studies of these defined microbial systems established the new field of ‘community proteogenomics.’ The linking of emergent ecological patterns in these communities to their molecular and evolutionary underpinnings also established a molecular paradigm for the predictive exploration and consequent explanation of behaviour in more complex microbial ecosystems.

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Beyond revealing new insights about the microbial biology and adaptive activities at play in these ‘contained’ biofilm systems, Banfield’s research is also highly relevant and widely needed for other fields including the unlikely pairing of ecological science and the mining industry.

“This is because the microorganisms involved also play key roles in promoting both the generation of acid mine drainage (a major environmental problem worldwide) via their geobiological effects and in bioleaching, which is relevant for potential low-energy alternatives for the recovery of metal resources from the drainage pits.”

Another ‘extreme’ environment under scrutiny by Banfield’s research group is the hypersaline Lake Tyrrell in Victoria, Australia. Here they are in the process of reconstructing genomes from microbial eukaryotic, bacterial, archaeal and viral populations collected across a variety of timescales, from hours, days, months to years.

The relatively low diversity of organisms able to survive in these conditions allows for complete or near-complete genome assembly from the dominant populations, and this information can then be used to unravel population heterogeneity and to characterise changes in population and community structure over time.

“With deeply sequenced metagenomes from a variety of organism types, along with geochemical data, we should be able to determine the ecological significance of changes at the population and community levels over short-term and longer timescales,” she says.

Putting it right

Another major topic of interest is bioremediation of contaminated environments, and the great potential of microorganisms in the subsurface to address issues, such as environmental contamination and climate change.

“Microbes have had billions of years to evolve an as yet unimagined suite of metabolic capabilities, some of which may provide opportunities to address pressing human needs,” Banfied says.

“In fact, we know essentially nothing about, arguably, half of the microorganism types on the planet. Now, developments in high throughput sequencing provide the opportunity to go far beyond profiling diversity to enable comprehensive evaluation of which microbes are where, and assessment of their metabolic potential and function in situ.

“In fact, community metagenomic methods generate hypotheses that can be tested. So, by first predicting the capacities of microorganisms in a given environment, then predicting which additives should elicit a response, and finally by conducting experiments to test these predictions, we may be able to design stimulation strategies that lead to new biotechnologies including for bioremediation.”

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Banfield’s team is part of a large, multi-disciplinary project in Colorado looking at the use of stimulated microbial activity for bioremediation of metal contamination in natural environments.

The overall goal of the project is to develop a mechanistic understanding of all the subsurface activities controlling the metal mobility, including microbial, with a focus on developing new scientific models that could benefit bioremediation strategies.

“Specifically, organic carbon is added to the field site subsurface to promote the growth of iron- and uranium-reducing bacteria. We then try to understand how microbial consortia change as ferric iron minerals are depleted and the community changes from iron to sulfate use.

“In other words, does the changing geochemical environment affect microbial strain makeup or metabolism, and are some strains better at metal remediation than others?”

Field and laboratory experiments conducted by the team working at the site use novel proteogenomics, stable isotope probing, chip arrays, and biogeophysical monitoring techniques to link microbial metabolic status and biogeochemical processes.

The public face of microbes

While in Brisbane for the ASM meeting, Banfield will also be presenting a public lecture to discuss her research and some of the many aspects that are of wider interest. She hopes that doing these sorts of talks gives the general public new insight into the microbial world as a whole and not just the one they typically think of as causing disease.

“I want the public to move their perception of microorganisms from ‘germs’ to ‘vital, integral components of the world around them’,” Banfield says. To this end, she will stress the existence and importance of connections between microbes and their surrounding: the atmosphere, climate, water quality and soil fertility, just to name a few.

“I will also probably talk about how microorganisms impact on human health. Indeed, we have co-evolved with our ‘microbiome.’ At birth, the human gut is sterile, and then over the first days, weeks and months of life, it is colonised. The process is critical for health and development, and aberration in microbial colonisation can lead to medical complications, including death.”

Banfield’s work in this space takes place in a Neonatal Intensive Care Unit (NICU), which is of, course, a relatively controlled environment. Several potential sources of microbes are examined along with the infants themselves with the goal of characterising the forces that shape the colonisation process in healthy infants.

“My hope is that in the future, we will recognise ourselves less as ‘humans’ and more as actual ‘ecosystems’ involving innumerable microbial partnerships and interactions.”

This feature appeared in the May/June 2012 issue of Australian Life Scientist. To subscribe to the magazine, go here.