Department of Biosciences, Rice University, Houston, Texas, USA.
Systems, Synthetic, and Physical Biology Graduate Program, Rice University, Houston, Texas, USA.
mSystems. 2024 Jan 23;9(1):e0096623. doi: 10.1128/msystems.00966-23. Epub 2023 Dec 7.
Microbes can be found in abundance many kilometers underground. While microbial metabolic capabilities have been examined across different geochemical settings, it remains unclear how changes in subsurface niches affect microbial needs to sense and respond to their environment. To address this question, we examined how microbial extracellular sensor systems vary with environmental conditions across metagenomes at different Deep Mine Microbial Observatory (DeMMO) subsurface sites. Because two-component systems (TCSs) directly sense extracellular conditions and convert this information into intracellular biochemical responses, we expected that this sensor family would vary across isolated oligotrophic subterranean environments that differ in abiotic and biotic conditions. TCSs were found at all six subsurface sites, the service water control, and the surface site, with an average of 0.88 sensor histidine kinases (HKs) per 100 genes across all sites. Abundance was greater in subsurface fracture fluids compared with surface-derived fluids, and candidate phyla radiation (CPR) bacteria presented the lowest HK frequencies. Measures of microbial diversity, such as the Shannon diversity index, revealed that HK abundance is inversely correlated with microbial diversity ( = 0.81). Among the geochemical parameters measured, HK frequency correlated most strongly with variance in dissolved organic carbon ( = 0.82). Taken together, these results implicate the abiotic and biotic properties of an ecological niche as drivers of sensor needs, and they suggest that microbes in environments with large fluctuations in organic nutrients (e.g., lacustrine, terrestrial, and coastal ecosystems) may require greater TCS diversity than ecosystems with low nutrients (e.g., open ocean).IMPORTANCEThe ability to detect extracellular environmental conditions is a fundamental property of all life forms. Because microbial two-component sensor systems convert information about extracellular conditions into biochemical information that controls their behaviors, we evaluated how two-component sensor systems evolved within the deep Earth across multiple sites where abiotic and biotic properties vary. We show that these sensor systems remain abundant in microbial consortia at all subterranean sampling sites and observe correlations between sensor system abundances and abiotic (dissolved organic carbon variation) and biotic (consortia diversity) properties. These results suggest that multiple environmental properties may drive sensor protein evolution and highlight the need for further studies of metagenomic and geochemical data in parallel to understand the drivers of microbial sensor evolution.
微生物可以在地下数公里的地方大量存在。虽然已经研究了微生物在不同地球化学环境中的代谢能力，但仍不清楚地下小生境的变化如何影响微生物感知和响应环境的需求。为了解决这个问题，我们研究了微生物细胞外传感器系统如何随不同深度微生物观测站（DeMMO）地下站点的宏基因组中环境条件的变化而变化。由于双组分系统（TCS）直接感知细胞外条件，并将此信息转化为细胞内生化反应，我们预计这种传感器家族会随着在生物和非生物条件上存在差异的地下贫营养环境而变化。在所有六个地下站点、服务用水对照点和地表站点都发现了 TCS，在所有站点中，每 100 个基因平均有 0.88 个传感器组氨酸激酶（HK）。与地表来源的流体相比，地下裂隙流体中的 TCS 丰度更高，候选菌门辐射（CPR）细菌的 HK 频率最低。微生物多样性的衡量标准，如香农多样性指数，表明 HK 的丰度与微生物多样性呈负相关（=0.81）。在所测量的地球化学参数中，HK 频率与溶解有机碳的变化相关性最强（=0.82）。综上所述，这些结果表明生态小生境的生物和非生物特性是传感器需求的驱动因素，并表明在有机养分波动较大的环境（如湖泊、陆地和沿海生态系统）中的微生物可能比养分较低的生态系统（如开阔海洋）需要更多的 TCS 多样性。
感知细胞外环境条件的能力是所有生命形式的基本特性。由于微生物双组分传感器系统将有关细胞外条件的信息转化为控制其行为的生化信息，因此我们评估了这些传感器系统在多个生境中如何在地球深处发生演变，这些生境的生物和非生物特性各不相同。我们表明，这些传感器系统在所有地下采样点的微生物共生体中仍然丰富，并观察到传感器系统丰度与非生物（溶解有机碳变化）和生物（共生体多样性）特性之间的相关性。这些结果表明，多种环境特性可能会驱动传感器蛋白的进化，并强调需要进一步平行研究宏基因组和地球化学数据，以了解微生物传感器进化的驱动因素。
