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A decade of interdisciplinarity

2016/03/07

Ten years ago this month, about 25 scientists from the Life Sciences and Earth Sciences convened in Avignon, France for the interdisciplinary meeting that set into motion the current international research dynamics on the role of microorganisms in atmospheric processes.  The meeting, funded by the European Science Foundation program for Exploratory Workshops, was romantically entitled Microbiological Meteorology: Working at the Intersection of Biology, Physics and Meteorology to Understand and Regulate the Microbial Component of Weather. (click here for the program, presentations and report).

IMG_4394

Participants of the 2006 ESF workshop on Microbiological Meteorology.

Front row (from the left): Zev Levin, Gabor Vali, David Sands, Cindy Morris, Christel Leyronas, Tom Hill. Back row: Ottmar Moehler, Laurent Huber, Dominique Courault, Roland Psenner, Paul DeMott, Ulirich Pöschl, Ruprecht Jaenicke, Dimitri Georgakopoulos, Heidi Bauer, Berhard Vogel (peeking over Heidi’s head), Mihaly Posfai, Janine Fröhlich-Nowoisky, Marc Bardin, Laurent Deguillaume, Bruce Moffett.

 

This meeting was followed by a flush of other meetings that consolidated this initial group of researchers and drew in others. This included a session on Biological Ice Nucleators in the Atmosphere – at the Crossroads of Physics and Biology at the General Assembly of the IUGG (Int. Union of Geodesy and Geophysics) in Perugia, Italy in 2007, a special session on Biological Aerosols at the International Conference on Nucleation and Atmospheric Aerosols in Prague in 2009 and another session on Biological Aerosols in the Earth System at the IUGG General Assembly in Melbourne in 2011. Since those initial meetings, and as a consequence of the collaborations and publications that resulted, the surge of interest in this field has been remarkable.

What has this decade of effort to build an international and interdisciplinary network really changed concerning the tools for exploring the influence of microorganisms on atmospheric processes and the knowledge resulting from this exploration? And what are the major challenges that should be a priority for the next decade? To put together answers to these questions, I combined my own opinions with those of some of the scientists who have the most active hindsight on this subject – in particular Gabor Vali, Zev Levin and Keith Bigg.

NEW TOOLS, NEW VOCABULARY, NEW INSIGHTS

We have expanded the scope of ice nucleation active particles of biological origin and confirmed their ubiquity. Various microorganisms, and especially numerous fungal species, have been added to the list of efficient (“warm-temperature”) ice nucleators. But, in addition, numerous studies have shown that particles with ice nucleation activity can be composed of various organic matter absorbed to inert mineral particles.  Rich, organic soils are one source of such particles.  This has led us to alter our vocabulary to adapt more generic expressions, such as Ice Nucleating Particles (INPs), to account for the variability in the nature of the particles. Furthermore, bio-INPs are ubiquitous: on plants, in fresh and marine waters, in precipitation, in leaf litter, in soils, and in clouds.

There has been a surge of proxies to identify INPs of biological origin. Based on the frequent use of heat sensitivity of ice nucleation activity in papers on biological INPs, it is clear that this has become the technical criterion for defining biological INPs. In parallel, particle fluorescence in UV-LIF spectrometers (such as the WIBS) has become a widely deployed criterion to identify biological particles in aerosols and in ice crystals. Probes (primers) for molecular detection (PCR) of the gene for the INA protein in Pseudomonas syringae and related bacteria have also been developed. But the sensitivity of this latter tool does not yet rival classical microbiological approaches.

Biological INPs have new rivals in the mineral world for efficient ice nucleation activity. Recently, the ice nucleation activity of feldspar was revealed, with the upper limits of the temperature of activity comparable to that for bio-INPs (near -5°C) making it the only mineral that rivals bio-INPs for this upper limit. However, in terms of the density of ice nucleation sites per surface of particles, bacterial INPs – and especially Pseudomonas syringae – still pack the greatest punch by several orders of magnitude.

Biological INPs have been “injected” into the realm of math and physics. Numerous models of cloud processes have included parameters that permit simulations of the effect of INPs having activities and abundances corresponding to those of biological INPs. This has led to the assessment of effects on cloud life-time, lightning, and precipitation.  Biological INPs have also been literally injected into cloud simulation chambers in order to catch these INPs in the act of inciting glaciation. The Snomax® product has proven to be a useful tool to allow scientists without access to microbiological labs to conduct such experiments.

Atmospheric microorganisms are also important in processes other than ice nucleation. The metabolic impact of microorganisms in the atmosphere has been a hotly debated subject because of the overriding importance of light-driven reactions in the chemistry of the atmosphere.  But, it has become established that there are conditions under which microorganisms surpass photochemistry or catalyze reactions not typical of photochemical processes.

A multitude of field observations have corroborated a role for biological INPs in precipitation. High altitude observatories and aviation-based sampling campaigns have provided much needed evidence that biological particles are guilty of being in the right places at the right time to be involved in processes leading to precipitation. The names of these sites and campaigns are becoming household words, such as Storm Peak, Jungfraujoch, Puy de Dôme, CalWater, etc. Results of these campaigns have revealed the possible importance of season and origin of air masses in the abundance of biological INPs.

Above all else, the atmospheric cycle of bio-INPs is now considered more seriously and a role for them in precipitation is assumed to be plausible.  A striking sign that this plausibility is being accepted is the more and more frequent use of the term “bioprecipitation” by physicists and biologists alike. The term is used mostly to describe the cycle in which microorganisms, mostly from plants, are transported to clouds, foster cloud glaciation and rainfall that deposits these microorganisms back on plants and also provides water for their subsequent multiplication. The past 10 years has seen an incredible complicity between Biology and Physics to provide evidence for the plausibility of some of the major processes of this cycle. Importantly, there have been several new reports about the rapid increase of INPs in the atmosphere shortly after rainfall and we have been reminded of the data on this phenomenon from as early as the 1950’s – all bolstering the occurrence of this important step of the bioprecipitation cycle. Mathematical tools have been made to assess the intensity of the feedback of rainfall in this cycle as a means to identify where rainfall is most sensitive to aerosols.

 

A RESEARCH COMMUNITY

Another important outcome of the past decade has been the creation of a research community. This community is not only interdisciplinary but it also includes scientists from several generations of research on ice nucleation and bio-INPs. As Gabor points out, this community is critical to assure continuity in research.  The long term efforts that will be needed to attain certain goals about the role of bio-INPs in precipitation are difficult to get funded as single, full projects.  Therefore, as a community we will need to continue stitching together the patchwork of our results and to try to collectively define the subsequent goals. The visibility and interest that we have created has managed to attract young people who have smartly tackled relatively short-term projects that are contributing to the long-term goals.

 

FUTURE CHALLENGES

The greatest challenge for the future is to provide solid, direct evidence for the importance of bio-INPs in precipitation formation. This will be very difficult mostly because of the inherent complexity of how the ice phase in general leads to precipitation in different cloud regimes. The nature and spectrum of action of bio-INPs is also highly variable and this adds on an additional dimension of complexity. Field observations have been one of the main foundations of the growing body of corroborative evidence and of the increasing plausibility of a role for bio-INPs in precipitation. But in the future will field experimentation be used to provide some of the needed solid evidence?  Would such field experimentation be another form of direct cloud seeding? Or rather, would we be able to deploy tools of modern molecular genetics and genomics to link sources, such as vegetation that harbors very specific types of microbial INPs, with these same microbial INPs in clouds, in ice crystals and in precipitation? The ubiquity of certain bio-INPs such as Pseudomonas syringae, Fusarium spp., lichens, etc. will, in fact, hinder such an approach. On the other hand, the extreme host specificity of rust fungi, that cause recurrent epidemics from clearly identifiable sources for which there are hundred-year historical records on most major continents, is one model of bio-INPs that could serve us well for this challenge. Because of the size of bio-INPs such as fungal spores, their action as giant cloud condensation nuclei (GCCN) might be a compounding factor in their role in precipitation. Keith points out that the interest in GCCN has not been proportional to their potential role in the bioprecipitation process and deserves more attention. Furthermore, ice nuclei are only important to rainfall production at temperatures below zero while GCCN can potentially stimulate precipitation in clouds at any temperature.

Another obstacle to advancing our understanding of the role of bio-INPs in the formation of precipitation is the continuing debate about the sufficient abundance of microbial INPs. Continued effort to expand the scope of biological INPs to include submicron-sized remnants of biological organisms, which are likely to be much more numerous than intact microbial cells and spores themselves, will probably greatly contribute to resolving this debate.

Unraveling the mechanisms and efficiency of transfer of bio-INPs from Earth’s surface to the atmosphere is also another important challenge. Methods to facilitate quantification of flux of bio-INPs from the ground into the atmosphere will be very welcome and will be an enormous technical leap.  In the meantime, mapping of the properties of near ground aerosols vs. the properties of bio-INPs on land surfaces across a wide variety of land covers and geographic sites might contribute to this challenge. Nevertheless, once bio-INPs are released from ground level sources, they age during transport in the atmosphere. Hence, questions about the transfer of bio-INPs into the atmosphere go beyond the basics of mass release as a function of wind, humidity and surface conditions and must address how the ice nucleation activity of bio-INPs is modified. Likewise, inert atmospheric particles with no inherent biological constituents might also pick up biological components during their transport. Zev reminds us that examples of such phenomena are starting to be suspected during the transportation of aerosols over oceans and during the flight of volcanic ash. In this light, there will be greater and greater need for techniques of detection and characterization of atmospheric INPs that can separate out the increasing range of classes of bio-INPs.

The upcoming generations of environmental scientists will be under considerable influence from the concern over climate change and its numerous ramifications. Sources of funding will probably mirror this concern with the likely consequence that research will be focused on macroscale processes. As much as such approaches are the path to direct evidence for the importance of bio-INPs in precipitation formation, understanding microscale processes will be needed to make better detection tools and for modeling. Gabor suggests that understanding the nature of nucleating sites and their permanent vs. transitory features is one aspect of microscale processes that should not be forgotten, in particular because of the dependence of quantitative laboratory analyses of ice nucleation activity on these features.

Future research should build on the past. Through online discussions in this network we have realized that there is a gold mine of research publications and competence from about 30-50 years ago that we probably have not build upon as best as we could have. Likewise for contemporary research findings, we need to use our convivial and dynamic network to anchor them into our collective knowledge, to frankly identify their strengths and deficiencies, and thereby continue building toward our ambitious long term goals.

 

 

 

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