Arsenic detoxification mediated by mutualistic cross-feeding in a thermophilic microbial consortium

Cyanobacteria-dominated microbial mats thrive in arsenic (As)-rich hot springs, but how they cope with As stress remains unclear. This study explored the As detoxification strategy of a photosynthetic microbial mat from a high-As hot spring in Tibet. The photosynthetic mat oxidized arsenite [As(Ⅲ)] under light without external organic carbon sources or electron acceptors. However, As(Ⅲ) was not oxidized by a pure culture of the dominant cyanobacterium isolated from the mat, "Thermoleptolyngbya sichuanensis" XZ-Cy5. Instead, exposure of a growing culture to 5 mM As(Ⅲ) led to rapid loss of chlorophyll and photosynthetic activity. In contrast, a pure culture of the mat-derived heterotroph Chelatococcus sp. XZ-Ab1 could oxidize As(Ⅲ) quickly with the addition of organic carbon and oxygen. A co-culture system demonstrated mutualistic interactions where "T. sichuanensis" XZ-Cy5 secreted organic carbon to facilitate heterotrophic growth of Chelatococcus sp. XZ-Ab1, while Chelatococcus sp. XZ-Ab1 promoted growth of "T. sichuanensis" XZ-Cy5 by oxidizing toxic As(Ⅲ) to the less toxic arsenate. Following growth of the co-culture using ¹³CO₂, NanoSIMS isotope tracing provided direct evidence of photoautotroph-derived carbon from "T. sichuanensis" XZ-Cy5 to Chelatococcus sp. XZ-Ab1. Metagenomic and genomic analyses indicated several mechanisms for metabolic complementarity between the two strains, including As detoxification by the heterotroph and fixed carbon and nitrogen provision by the cyanobacterium, in addition to oxygen production. Our findings reveal a cooperative survival strategy in extreme environments and provide a novel model for engineering synthetic microbial consortia for As bioremediation.