Why does soil inoculation work if soil microbes are such great dispersers?

 
 
 

Dr. Jasper Wubs

Postdoctoral Fellow, ETH Zürich, Switzerland

 
 
 
 

This has been something I have been wondering for a while. I hope you are not disappointed, but I don’t have the answer. I have not yet found time to do active research on it. Still it is one of the things in soil ecology that mystify me – or maybe I am just missing something obvious?

Let me explain.

In 2016, we published the results of a field experiment where we inoculated large plots with soil from donor areas that lay a few kilometres away (1). The idea was that the introduced (late-successional) soil microbiomes would induce positive soil feedbacks in the co-introduced plants, and indeed they did. Buy why? Why did we need to introduce them?

Fig. 1. Aerobiome sampler on top of a campus building (Credit Arjen de Groot).

Every microbiologist knows the statement ‘everything is everywhere, but, the environment selects’ introduced by Baas Becking (1934; 2), where the first part refers to the (near) universal dispersal ability of microbes. In fact, Baas Becking thought of microbes as aerial plankton (‘lucht plancton’). Many microbes have adaptations that facilitate transport through the air. Many form spores (many fungi and protists) and many have thick cell walls to protect from high UV radiation (e.g. Firmicutes).

Indeed, many bacteria, fungi and protists surf the airwaves. Recently, I was lucky enough to participate in a study with two of my science friends, Arjen de Groot and Stefan Geisen, where they installed a contraption (Fig. 1) that sucks microbes from the air and sequenced them (3). It turns out that even if you do this only for 21 days on top of a rather plain university building you can find a lot of microbes! In terms of species (or actually OTUs) we found 1230 bacteria, 1384 fungi, and 68 protists. The latter included several important plant and animal (invertebrate) pathogens. Like the soil, the aerobiome is highly diverse! (and potentially dangerous.)

With the recent revolution in sequencing technology, we can now identify microbes at much finer resolution, and this provides part of the answer to my question. Baas Becking was right that many microbes travel the airwaves, but few are pan-global. From detailed sequencing studies it is now clear that spatial patterns do exist in microbes (4,5), where some are found here and not there (biogeography in jargon). If we look deep enough, we see that each microbe is far from everywhere. But that is not the whole story.

While there are regional differences in microbial species composition, microbes do travel far. They have what is called a fat-tailed distribution (or dispersal kernel). While most don’t venture too far from their origin, a rather large and significant fraction do travel to the far end of their distribution curve (hence the fat tail). This curve is governed by Reynolds numbers and the viscosity of air and it turns out that spores or cells smaller than 40 μm diameter have the critical size for nearly unlimited dispersal through air (6). (For a beautiful and accessible explanation read Steven Vogel’s (1983, Princeton) Life in Moving Fluids: The Physical Biology of Flow.) Below this size, microbes float in air. This starts to sound like lucht plancton.

Fig. 2. Snow profile sampled at Jungfraujoch (Switzerland) showing Sahara dust as brown bands in the snow. In the bands, 100s of bacterial species were discovered that originated in Algeria (Credit Meola et al., 2015).

Fig. 2. Snow profile sampled at Jungfraujoch (Switzerland) showing Sahara dust as brown bands in the snow. In the bands, 100s of bacterial species were discovered that originated in Algeria (Credit Meola et al., 2015).

Indeed, empirical observations corroborate the physics. I don’t know of an equivalent study in microbes, but for peatmosses (Sphagnum; spores 20-45 μm) Sebastian Sundberg collected spore samples along a string of increasingly remote islands in Scandinavia and still found 1000 spores/m2/yr on an island (Svalbard) 1000 km from the nearest source and calculated that 1% of spores are expected to travel intercontinentally! (7). In another study it was shown that the Sahara dust raining down in European winters carries many bacteria (Fig. 2; 8). In the snowpacks of the Swiss Alps they discovered 100s of bacterial OTUs in dust that came from south-central Algeria: a net distance of some 1800km! (the computed air trajectory was at least twice as long.)

However, spore size is not everything. In a trap-culture study with ectomycorrhizal fungi (spore diameter ~10 μm) on a single host plant (Pinus muricata) in California they found spatial patterning within a kilometer (9)! Trap plants placed more than one kilometre from potential sources were frequently not colonized, including by Suillus species that in other studies were described as major long-distance dispersers. Maybe the discrepancy between studies arises from the effect of time? The trap-cultures were out trapping for six months and ectomycorrhizal spores can be dormant for some time. Maybe it was due to priority effects of other species colonizing the plants first? I don’t know.

In any case, it seems that many of the microbes introduced via soil inoculation should have no trouble, given sufficient time, to cover the few kilometres that lie between our donor and recipient sites. The donor sites are frequently disturbed by management and wild boar, leading to patches of bare soil and so the microbes should readily and frequently be able to join the aerial highways. The same goes for many other inoculation studies. Why don’t they make it?

Maybe it is the second part of Baas Becking’s statement and the local environment is not conducive to those microbes? But how does that square with the positive feedback among (late-successional) microbes and plants that drove our original field experiment? Should those feedbacks not ensure microbial establishment and local spread once they arrive?

This is the puzzle I am stuck on. The hypothesis I have come up with: maybe multiple interacting microbes (consortia) need to arrive more or less simultaneously to generate the positive soil feedbacks and this becomes increasingly unlikely with distance and number of necessary microbial partners.

I am curious to hear what you think – especially if you did spot the obvious thing that I missed! Do send me a mail! 

References

  1. Wubs ERJ, Van der Putten WH, Bosch M, Bezemer TM. Soil inoculation steers restoration of terrestrial ecosystems. Nature Plants. 2016;2:16107. doi: 10.1038/NPLANTS.2016.107

  2. De Wit R, Bouvier T. “Everything is everywhere, but, the environment selects”; what did Baas Becking and Beijerinck really say? Environ Microbiol. 2006;8(4):755-758. doi: 10.1111/j.1462-2920.2006.01017.x

  3. De Groot GA, Geisen S, Wubs ERJ, et al. The aerobiome uncovered: multi-marker metabarcoding reveals potential drivers of turn-over in the full microbial community in the air. Environ Int. 2021;154:106551. doi: 10.1016/j.envint.2021.106551

  4. Green J, Bohannan BJM. Spatial scaling of microbial biodiversity. Trends Ecol Evol. 2006;21(9):501-507. doi: 10.1016/j.tree.2006.06.012

  5. Bates ST, Clemente JC, Flores GE, et al. Global biogeography of highly diverse protistan communities in soil. ISME J. 2013;7(3):652-659. doi: 10.1038/ismej.2012.147

  6. Wilkinson DM, Koumoutsaris S, Mitchell EAD, Bey I. Modelling the effect of size on the aerial dispersal of microorganisms. J Biogeogr. 2012;39(1):89-97. doi: 10.1111/j.1365-2699.2011.02569.x

  7. Sundberg S. Spore rain in relation to regional sources and beyond. Ecography. 2013;36(3):364-373. doi: 10.1111/j.1600-0587.2012.07664.x

  8. Meola M, Lazzaro A, Zeyer J. Bacterial Composition and Survival on Sahara Dust Particles Transported to the European Alps. Front Microbiol. 2015;6:art1454. doi: 10.3389/fmicb.2015.01454

  9. Peay KG, Schubert MG, Nguyen NH, Bruns TD. Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol Ecol. 2012;21(16):4122-4136. doi: 10.1111/j.1365-294X.2012.05666.x

 
GSBI