Microbiome engineering optimized by Antarctic microbiota to support a plant host under water deficit

Authors: RODRIGUEZ, RODRIGO - Universidad De La Frontera; BARRA, PATRICIO - Universidad De La Frontera; LARAMA, GIOVANNI - Universidad De La Frontera; CARRION, VICTOR - Leiden University; DE LA CRUZ MORA, MARIA - Universidad De La Frontera; Hale, Lauren; DURAN, PAOLA - Universidad De La Frontera

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/24/2023
Publication Date: 9/15/2023
Citation: Rodriguez, R., Barra, P.J., Larama, G., Carrion, V.J., De La Cruz Mora, M., Hale, L.E., Duran, P. 2023. Microbiome engineering optimized by Antarctic microbiota to support a plant host under water deficit. Frontiers in Plant Science. Article 1241612. https://doi.org/10.3389/fpls.2023.1241612.
DOI: https://doi.org/10.3389/fpls.2023.1241612

Interpretive Summary: Microbiome is the term used to describe the suite of microorganisms living together in any given habitat. Root-associated microorganisms can enhance the tolerance of plants to water deficit and these associations are critical under extreme environmental stress. This work evaluated the capacity of specialized microbiomes in soil samples from the oldest, coldest, and driest desert on Earth, Antarctica, to co-evolve with tomato plants impacted by water deficit. Following treatment with Antarctic soils containing unique microbiome and two years of repeated transfer, tomato plants grown under water deficit with the specialized microbiomes had higher yield and lower stress indicators than those which were never inoculated with Antarctic soils. Notably, Bacillus bacterial species and a type of archaea, microorganisms known to exist in extreme environments, were unique to the microbiomes in soils from the Antarctic desert that helped the tomato plants thrive. These findings suggest strategies to enhance crop drought tolerance via the development of new lines of biological agricultural products based on unique microbiomes.

Technical Abstract: Agricultural productivity is an economic, social, and environmental necessity for human beings. However, the future of agricultural production faces many challenges in the current scenario of global climate change. Scientists have proposed that the plant microbiome offers numerous benefits to reduce or even alleviate (a)biotic stresses. Here, we investigated the cry for help phenomenon, a stress response of plants involving host-mediated microbiome engineering, using soil transplant as a potential strategy to improve water deficit tolerance in tomato plants. For this, tomato seedlings were used as a crop model with high sensitivity to water deficit and considerable economic importance. Antarctic soils are arid, so soil microorganisms are likely to be acclimated to dry conditions and provided the extreme environment, plant-microbe relationships may be especially vital for plants. Soils from five sites from Antarctica region (Yelcho station, Coppermine Peninsula, Fildes Bay, Arktowsky station and Deception Island) were used as donor of microbiomes and mixed with a Andisol (used as receptor soil). Tomato seedlings were grown and subjected to water deficit stress in a multigenerational approach over 10 cycles (10 generations i.e., 2 years). The induced stress was quantified by the level of chlorosis based on basis of a Matrix Scale Based (MSB) and leaf proline content. Rhizobacterial communities at 4 points of multigenerational selection were analyzed using metabarcoding techniques, using the region V3-V4 16s rRNA. Our results show that the soils from Fildes Bay mixed with Andisol soils (R+F) show higher tolerance to water deficit stress after multigenerational recruitment. Metabarcoding results suggested that Candidatus nitrocosmicus (archaea) and Bacillus spp. (bacteria) could be key microorganisms for the enhanced water deficit tolerance in tomato seedlings. Our study shows that the incorporation of a microbiome from an extreme environment (Antarctic soils) combined with host-mediated microbiome engineering could represent a promising strategy to modify the native microbiomes of agroecosystems to benefit crop hosts.