A leaf in the leaf: making photosynthesis on the leaf may sometimes not involve the plant

The plant is a complex ecosystem: The plant itself is something that everybody can see and touch, it lives however surrounded by deleterious as well as beneficial microbes. Plant life and microbe life are so tightly bound together that recent studies have created the term holobiont to identify the ensemble of all microbial communities plus the plant.
Many other studies have reported that without microbe contribution, the plant health can be severely impaired. This means that all the feeding crops like rice, wheat, soybean etc. need the right microbial communities in the right place, at the right moment, in order to be healthy and productive. These are the reasons why I am studying microbial communities associated to the plant, otherwise known as microbiome.

Of course, I am not the first one approaching this matter, and lot of new features have been discovered already concerning the steering mechanisms of microbiome interaction within holobiont.
However, some scientists recently have pointed out that some calculations do not add up. They have shown that the microbes known so far within microbiome, alone, do not explain the phenomena observed on the plant. For example, it has been found that a very common pathogen for Arabidopsis thaliana (a model plant), (Albugo, a parasitic oomycete), despite its visible impact on the plant, is responsible only for the 10% of microbial diversity. Other factors explain further microbial variation, but still they leave more than 40% of microbial diversity without an explanation.

I then hypothesized that this gap may be explained by the presence of other kind of microbes. Microbes that so far have been neglected. I called them overlooked microbial eukaryotes, and with this name I mean to encompass all eukaryotic microbes which are neither fungi, nor plants, nor oomycetes. This includes an incredible number of organisms which are well known in other contexts, however never studied on the plant. For example amoebas, plasmodial parasites, small animals, or microalgae.
What my findings recently showed, is that microalgae have a prominent role in shaping bacterial and fungal diversity associated to plants.

In order to disentangle this better, I collected samples of natural Arabidopsis thaliana in different locations (France, Spain, Sweden, and Germany) and different ecosystems (parks, cliffs, mountains, even towns). And in all these locations and habitats, algae were present, mostly on the leaf surface, but also inside the leaf. These findings raise an apparent paradox: what are photosynthetic organisms like algae doing on top of an organism, which is the archetype of photosynthesis (the plant)?
In order to tackle this question, I narrowed down few candidate species among microalgae. What I found is that they seem to explain a large portion of that unknown variation that remained unexplained before. Few of these candidates allegedly form lichens (symbiosis with fungi), on the leaf surface, but some of them also inside the leaf tissue. Some other seem to be tightly bound to some bacteria, likely engaging a mutualistic interaction.

These findings disclose for the first time that the microbiome world within plant holobiont is much wider than expected and still to be explored. And also, that by studying the ecology of microalgae associated with plants we could one day add a substantial piece to the plant holobiont puzzle.

Proceeding in investigating the plant holobiont is something fascinating that has been shown to be able to contribute in sustainable crop cultivation and food production. However, it is something complex that needs a lot of different expertise to come together, from the ecology, to the informatics, statistics, metabolomics, and in exchange, it is a field that can provide insights useful to many experts in different fields. CEPLAS was the perfect frame in which to tackle this study. Its orientation to achieve knowledge in sustainable agriculture and the presence in it of many top-level professionals and experts in the cited field helped me greatly in achieving my goals and contributing to open a new field of research.

Planter’s Punch

Under the heading Planter’s Punch we present each month one special aspect of the CEPLAS research programme. All contributions are prepared by our young researchers.

Further Reading

Agler, M.T., Ruhe, J., Kroll, S., Morhenn, C., Kim, S.-T., Weigel, D., and Kemen, E.M. (2016). Microbial Hub Taxa Link Host and Abiotic Factors to Plant Microbiome Variation. PLOS Biol. 14, e1002352. [link]

Berendsen, R.L., Pieterse, C.M.J., and Bakker, P.A.H.M. (2012). The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478–486. [link]

Hassani, M.A., Durán, P., and Hacquard, S. (2018). Microbial interactions within the plant holobiont. Microbiome 6, 58. [link]

About the Author

The article was written by Alfredo Mari, who is a CEPLAS doctoral researcher. By the use of metagenomic tools and molecular biology analyses he aims to understand mechanisms of mutualistic interactions between pathogenic and non pathogenic protozoa in biofilms that shape the foliar microbiome.

 

 

Heinrich Heine University
University of Cologne
Max Planck Institute for Plant Breeding Research
Forschungszentrum Jülich