Category Archives: H2 Soil Microbiology

Soil microorganisms utilize H2 from the atmosphere so strongly as to comprise its largest sink; however, many fundamental questions surrounding this process remain. Which microorganisms possess the ability to utilize atmospheric H2 at such low concentrations (~500 ppbv)? What, if any, competitive advantage is gained via access to the atmospheric H2 reservoir? Which environmental processes most strongly influence the rate of H2 uptake by these microorganisms?

We hope to contribute to our understanding of these questions with our explorations into the microbiology of H2 uptake at Harvard Forest.

Soil systems – the challenges of complexity and scale

Soils are complex systems, in which physical, geochemical and biological processes interact in aggregate structures situated in dynamically shifting air- and water-filled spaces. It is difficult to adequately sample soil properties and to model processes related to those soil measurements. These challenges were discussed in a stimulating three-day conference on Complex Soils Systems in Berkeley a few weeks ago. Attendees came from an incredible diversity of backgrounds with a common interest in tackling issues in soil science. The need to better understand soils was motivated by the importance of soil processes in climate and for figuring out “How to feed the soil and the planet?” in the anthropocene – a question posed early on by Professor John Crawford. 

Issues of scale were brought up explicitly or were evident implicitly in many of the presentations. Namely, that relevant processes in biogeochemical cycles occur over a wide range of spatial (nano- to mega-meter) and temporal (seconds to millennia) scales, but our observations are typically limited to a much narrower scope given measurement and resource constraints. These issues were elegantly summarized in the recent article “Digging Into the World Beneath Our Feet: Bridging Across Scales in the Age of Global Change” by Hinckley, Wieder, Fierer and Paul in Eos, Transactions American Geophysical Union 95 (11), 96-97. In a real sense, the scale issue presents problems when societal decisions regarding soil sustainability and ecosystem services are made using data and models derived from different (often smaller) spatial scales than are relevant to the policies and issues themselves.

One illustration of the concept of a spatially complex soil system is illustrated with the figure below by California College of the Arts (CCA) student Sakurako Gibo. The image depicts a theoretical assemblage of soil microbes with different morphologies (for instance round spores versus string-like mycelia). In the second figure, the complex system is “pulled apart” into bins that might represent the effect of a sampling strategy that subsamples components of the whole system. The information about the original complex assemblage and connections is not retained, and as a result, data and rules based off of the binned samples may be different from the case in the real intact community.

Spatially complex microbial community

Spatially complex microbial community

Spatial ordering is lost in measurements and models

Spatial ordering pulled apart

What to do? I walked away from the meeting in awe of the amount of unanswered questions on soil complexity and scale. However, with the increasing technical capability in soil and microbial measurements, and efforts at meetings like this one, made it evident that progress will continue in this area.

I’ll end with another neat set of figures produced by CCA student Leslie Greene who illustrated an emergent pattern of predicted H2 consumption (o) based on the availability of H2 (•) from the atmosphere (distributed) and from N2-fixing root nodules (gray filled circles). She created the pattern of H2 consumption based on one rule, soil moisture had to be above 10% and below 50%, as indicated by the concentric rings around water-logged soil sites (red filled circles). From this simple scheme, an irregular pattern emerges of the location where H2 consumption occurs. When faced with the complexity of soil, it is easy to feel paralyzed, and perhaps starting with a simple approach like this will help me embrace the system and its questions.

Emergent H2 system

Emergent patterns of H2 consumption

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At a slightly more macro scale

Thank you for the BioDesign course organizers at California College of the Arts (Tobi Lyn Schmidt and Mike Bogan)!

Undergraduate Researcher Shersingh’s SURGE Experience

Congratulations to visiting undergraduate researcher Shersingh Joseph Tumber-Davila on completing and thriving in the demanding eight-week Summer Undergraduate Research in Geoscience and Engineering (SURGE) program! Shersingh came to the Welander lab with a strong background in environmental research (news article) from his home institution of the University of New Hampshire. SURGE is a competitive earth science research and graduate school preparation program, which is specifically designed to recruit students of diverse backgrounds from other universities across the country. I was amazed at the number of activities the program had for the students including GRE test preparation, faculty seminars, career and grad school panels, and field trips. This was all while performing graduate-level research including a oral and poster presentation at the end of the program. Shersingh approached all these demands with amazing energy and attitude, which we’d really like acknowledge!

SURGE student Shersingh

SURGE student Shersingh

In Shersingh’s research, he asked whether microbe-mediated hydrogen (H2) uptake support C mineralization in soils. Soils are a strong sink for atmospheric H2, which is presumably used by soil microorganisms to fuel their energy metabolism. In addition, emissions of H2 have grown since the industrial revolution, so the availability of H2 energy to soil microbes likely also increased. Shersingh tested the influence of excess H2 on the ability of soil microbes to mineralize soil carbon for a variety of carbon substrates, especially those that can be energy intensive (e.g., lignin and lignocellulose). He used Streptomyces ghanaensis as a model organism containing high affinity hydrogenase (H2 uptake) and laccase (lignin breakdown) genes. By measuring carbon dioxide respiration rates and intermediate products involved in the breakdown of lignin and lignocellulose, we found evidence for increased breakdown of lignocellulose (straw) with elevated levels of H2. This may point to a  link between the H2 and C biogeochemical cycles in soils that will be interesting to pursue further. This project is in collaboration with Stanford postdoc Marco Keiluweit who specializes in soil carbon cycling.

BioDesign course – bridging science and art

Biologist/architect team Tobi Lyn Schmidt and Mike Bogan created a course linking artists, designers, architects, and biologists from the California College of the Arts (CCA) and Stanford University. I served as a postdoc mentor to help inspire and guide the process of cross-hybridizing biology and design (some examples) with three really talented undergraduate CCA students: Leslie Greene, Sakurako Gibo, and David Lee.

The students were first charged with creating designs to illustrate scientific concepts in my field of research. I challenged them think about the issue of scale with respect to the biogeochemical cycles I study. The processes I investigate occur over a wide range of spatial and temporal scales, which is a challenge for their measurement and interpretation. David focused on a selection of atmospheric trace gases with a wide range of abundances, and that interact with each other through key reactions. In his image, the hydroxyl radical (OH) is illustrated by the white dot from which orange and blue strings respectively represent the path length to molecules of  hydrogen (H2) and methane (CH4) in the surrounding space. The density of the strings is representative of the concentration of H2 and CH4 relative to OH. I love the sense of competition in this image. These reduced molecules compete for reaction with OH, and with other trace gases not shown, which helps explain the relatively their long lifetimes of H2 (~2 years) and CH4 (~10 years) in the atmosphere.

Concentration Burst, by David Lee

Concentration Burst, by David Lee

The second task for the students was to manipulate a biological system for design or artistic ends. All three students visited the Welander geobiology lab at Stanford and the Berry lab at Carnegie on campus where atmospheric trace gases are measured. For her project, Leslie was interested in manipulating microorganisms to reveal art. Using a combination of strains from the lab and purchased online, Leslie created competitive interactions between organisms and against antibiotics to reveal structures that were both patterned and complex. In the example below, she laid a cross-pattern of Streptomyces ghanaensis and Bacillus subtilis colonies and let them grow and compete. Intriguing features arose, appearing as if the Streptomyces strain grew on top of the Bacillus strain, perhaps antagonistically or not. Leslie overlaid emergent patterns in topology and color from microbial cultures with and without competition to create an amazing image that reveals some very aesthetic order in the systems.

Bio-manipulation of Streptomyces ghanaensis and Bacillus subtilis

Bio-manipulation of Streptomyces ghanaensis and Bacillus subtilis

Emergent patterns from competition

Emergent patterns with and without competition

 

Finally, the students illustrated various concepts related to my work including artistic renditions of Streptomyces colonies and concepts of complexity (see related post). I really love the feel of the image created by Sakurako Gibo showing the atmospheric H2 concentrations that I measured between the ground and top of a measurement tower (y-axis) over the year-long experiment (x-axis) at Harvard Forest as an ephemeral curtain. Higher concentrations of H2 are represented with a deeper intensity of blue. The impact of the soil sink is illustrated by the lightening of the color near the base of the image caused by high rates of soil microbial H2 consumption in summer and fall.

Curtain of H2 Harvard Forest

Curtain of H2 at Harvard Forest, by Sakurako Gibo

 

Manuscript on consumption of atmospheric H2 during the life cycle of soil-dwelling actinobacteria

The presence (left) or absence (right) of aerial hyphae in Streptomyces may influence their atmospheric H<sub>2</sub> consumption

The presence (left) or absence (right) of aerial hyphae in Streptomyces may be linked to atmospheric H2 consumption

Microbe-mediated soil uptake is the largest and most uncertain variable in the budget of atmospheric hydrogen (H2). In a recent study (early view in Environmental Microbiology Reports), we probed the advantage of atmospheric H2 consumption to microbes and relationship between environmental conditions, physiology of soil microbes, and H2First, we were interested in whether environmental isolates and culture collection strains with the genetic potential for atmospheric H2 uptake (a specific NiFe-hydrogenase gene) actually exhibit atmospheric H2 uptake. To expand the library of atmospheric H2-oxidizing bacteria, we quantify H2 uptake rates by novel Streptomyces soil isolates that contain the hhyL and by three previously isolated and sequenced strains of actinobacteria whose hhyL sequences span the known hhyL diversity. Second, we investigated how H2 uptake varies over organismal life cycle in one sporulating and one non-sporulating microorganism, Streptomyces sp. HFI8 and Rhodococcus equi, respectively. Our observations suggest that conditions favoring H2 uptake by actinobacteria are associated with energy and nutrient limitation. Thus, H2 may be an important energy source for soil microorganisms inhabiting systems in which nutrients are frequently limited.

Much of this work was done with the help of Deepa Rao, an undergraduate researcher at MIT at the time who wrote an award-winning senior thesis on the topic and presented results in a number of venues, including at AGU 2012.

 

Deepa blogs about AGU 2012

Connecting H2 consumption to life cycles of soil microbes

Deepa’s AGU Poster “Connecting H2 consumption to life cycles of soil microbes”

Read Deepa Rao’s Blog Post

It’s a wonderful piece (highlighted on the EAPS department website) about her first the AGU experience written through her uniquely balanced scientific and artistic perspective. For example, she writes, “Science, nature, life, emergence, and the universe have always inspired my art. And it is the unnecessary beauty of science that makes it deeply mysterious and so inviting to my mind… AGU was an incredible week of reconnecting with friends, advisors, professors, fellow researchers. It was also unexpectedly a way for me to connect a path to a foreseeable future where my two passions can be combined, perhaps even muddled, into an exciting career.”

Thesis Defense!

I defended my thesis entitled “Field Measurement of the Fate of Atmospheric H2 in a Forest Environment: from Canopy to Soil” on October 4, 2012.

It was an incredible relief to finish the thesis document itself (link to .pdfCarl-Gustaf Rossby Prize for best PhD thesis in PAOC for the year). I really enjoyed preparing and giving my thesis defense presentation. It’s not often that one gets to present the culmination of six years of hard work and personal development to colleagues, family, and friends. I am grateful for mentorship from my advisor Ron Prinn, my thesis committee (Steve Wofsy – Harvard, Bill Munger – Harvard, Tanja Bosak – MIT, Colleen Hansel – WHOI, Shuhei Ono – MIT), and many others along the way!

I am continuing at MIT for a short (approximately 9 month) postdoctoral position with Ron Prinn to translate the work described in my thesis to publications. I am currently exploring possibilities for a postdoctoral position at the intersection of microbial ecology and atmospheric chemistry (trace gas cycles or aerosols) by searching advertised positions and writing fellowship proposals.

ISME 14 – The power of the small

Last week I attended ISME 14 (International Symposium on Microbial Ecology) in Copenhagen, Denmark. It was a delight to see the city – its juxtaposed giant modern, cool, sterile buildings surrounding the historic old city. More of a delight was unexpectedly running into friends from the MBL Microbial Diversity summer school (2010) and realizing they are now my colleagues.

Presenting a poster that Deepa Rao and I co-authored on the “Physiology of the microbe-mediated soil sink for atmospheric H2” at ISME in Copenhagen, Denmark.

The conference itself was quite good. I appreciated the range of content from very big picture and abstract to focused experimental projects. One message I took away from the community was a sort of -omics backlash, or perhaps whiplash, to the idea that generating more and more -omics data is the sole future for microbial ecology. It seems that presenters coming from both the -omics and experimental side were acknowledging the importance of both tools, and especially of using them together. Those seem to be a lot of tools for any one scientist to master, so I am encouraged that the tone was of collaborative holistic approaches for tackling scientific questions.

Wind turbines and modern architecture outside of Copenhagen

I really enjoyed a somewhat unique session. It was a discussion entitled “Frontiers in microbial ecosystem science: Energizing the research agenda” sponsored at this and other conferences by the US National Science Foundation. All sorts of issues were raised in a discussion of “what needs to be done” – what are the important topics and how should we advance microbial ecology. I was struck by how strong the arguments were that microbial ecology is important for understanding, and possibly mitigating, climate change. This is my main interest, but I often find the microbial ecology literature and research interests so focused on minute points (I think my own project included), that it is difficult to see the link between the microbial and global scales. At this session I learned that it is not only because it is difficult to do, but also because the funding agencies seem to push scientists to write grants in one or the other. It is difficult to be interdisciplinary (falling under more than one NSF department). It has been a (fun) challenge for me to try to get a foot in both atmospheric and microbial ecology science, and it was encouraging to hear from the community that the intersection of the two is valued.

Tuborg beer and the Royal Copenhagen porcelain company

Deepa receives Goetze Prize for Undergraduate Research

At the 2012 EAPS Student Awards Ceremony Deepa Rao received the Christopher Goetze Prize for Undergraduate Research for her thesis entitled : “Exploring the Microbe-mediated Soil H2 sink: A lab-based study of the physiology and related H2 consumption of isolates from the Harvard Forest LTER.” The award recognizes “ innovative experimental design, care in data collection, and sensitive application of results to research problems.”

Click here for a description of her Senior Thesis Presentation 

It has been a pleasure to supervise Deepa’s thesis research and her results will contribute to our research efforts to understand the mechanisms driving the soil sink for atmospheric H2. Professor Ron Prinn acts as the faculty advisor for both Deepa and I.

Deepa Rao accepting the award from her academic advisor Sam Bowring

Feature in EAPS article: Atmospheric chemistry redux

Atmospheric Chemistry Redux

MIT Department of Earth, Atmospheric and Planetary Science article describing the expansion of the atmospheric chemistry program at MIT over the past five years with a short feature on our work to understand the H2 soil sink in the field and in the lab.

Atmospheric H2 energetic fertilization to soil microorganisms in a forest ecosystem

I presented a poster at the at the Ecology of Soil Microorganisms conference in Prague, 2011 on the role of soil microorganisms in dominating the fate of atmospheric molecular hydrogen (H2). Recent work has linked atmospheric H2 uptake to a novel high-affinity [NiFe]-hydrogenase expressed in active Streptomyces sp. cells, and is perhaps not driven by abiotic hydrogenases as was previously thought. Consequently, atmospheric hydrogen may be a 60-85 Tg yr-1 energetic supplement to microbes in Earth’s uppermost soil horizon. To understand the role of this supplement to the soil microbial ecology, this work explores the following questions:

  1. What is the importance of atmospheric H2 energy to soil microbial communities relative to carbon substrates?
  2. How might this energetic supplement change with changes in anthropogenic H2 emissions?
Ecology of Soil Microorganisms poster

Ecology of Soil Microorganisms