Synergistic response of extremophiles in cyanobacterial crusts against in-situ exposure to multiple stratospheric stresses

Abstract

Abstract Background The stratosphere, with its harsh conditions similar to the Martian surface, provides a unique and relatively accessible environment for studying the adaptation of extremophiles in anticipation of extraterrestrial colonization applications. However, we are just beginning to understand the synergistic response of microbial communities under this Mars-like near space. Using cyanobacterial crusts from deserts, as a multitrophic model system, we loaded it on a balloon-borne astrobiology platform for direct exposure to multiple stratospheric stresses such as high radiation and extreme temperature fluctuations. We then performed multi-omics analyses to delineate the underlying composition alterations and metabolic response at the community level. Results After short-term in-situ exposure, a significant shift in the community composition of active members was observed that the relative abundance of photoautotrophs declined while chemotrophic abundance increased. We tracked the changes in metabolic processes against the stratospheric ambiance and found that life history strategies associated with resource acquisition, growth potential, and stress tolerance were regulated distinctively in different microbial categories. For instance, α-proteobacteria and chloroflexi tended to enhance the strategies related to the ability of stress tolerance, while actinobacteria assigned more resources to reinforce their growth potential. Cyanobacteria contributed to the promotion of different strategies, indicating their significant adaptability differentiation. Moreover, we demonstrated the unique thriving of Scytonema, a diazotrophic genus of cyanobacteria, attributed to its synthesis of anti-ultraviolet scytonemin, diverse material, and energy acquisition. These synergistic responses further induced interspecies mutualistic nutrient interactions, thus promoting the retention of organic carbon and nitrogen within the community, finally maintaining the stability of biocrusts in extreme environments of the stratosphere. Conclusions Our study underscores the adaptive resilience of cyanobacterial crusts under stratospheric conditions, with a notable shift in microbial composition and metabolic strategies. The robustness of Scytonema, particularly its unique survival capabilities, highlights its potential for extraterrestrial colonization. These findings expand our understanding of microbial proliferation in extreme environments, providing valuable insights for future astrobiological endeavors.