Ecological diversity and metabolic strategies of widespread Marinisomatota in global oceans

Marinisomatota (formerly recognized as Marinimicrobia, Marine Group A, and SAR406) are ubiquitous and abundant in marine environments, traditionally characterized as heterotrophic microorganisms. However, certain members of Marinisomatota have demonstrated the capacity to harness light for carbon dioxide fixation and the synthesis of organic compounds, thriving in the translucent zone or transitioning between the translucent and aphotic layers. The metabolic strategies driving the shift in trophic behaviors, and the factors influencing these transitions, remain largely unexplored. In this study, we investigate the metabolic strategies, ecological distribution, and dietary patterns of Marinisomatota through the analysis of metagenomic and metatranscriptomic data sourced from the global open oceans. A total of 1,588 Marinisomatota genomes were retrieved, representing one class, two orders, 14 families, 31 genera, and 67 species. These organisms are predominantly found in low-latitude marine regions, with relative abundances ranging from 0.18 to 36.21%. Among the 14 families, S15-B10, TCS55, UBA1611, UBA2128, and UBA8226 exhibit potential for light-dependent processes associated with Crassulacean acid metabolism (M00169). Three distinct metabolic strategies were identified within Marinisomatota: MS0 (photoautotrophic potential), MS1 (heterotrophic with a pronounced glycolytic pathway), and MS2 (heterotrophic without glycolysis). The emergence of these metabolic strategies may be a response to nutrient limitations within the ocean. This study reveals the potential for mixotrophic strategies in Marinisomatota, underscoring the critical interplay between life history traits and metabolic strategies in the evolution of novel nutritional groups.