关键词: Allochromatium vinosum anoxygenic photosynthesis cytochrome iron sulfur cluster purple sulfur bacteria pyrite transcriptomic sequencing

Mesh : Sulfides / metabolism Sulfur / metabolism Autotrophic Processes Iron / metabolism Chromatiaceae / metabolism genetics growth & development Electrons Bacterial Proteins / metabolism genetics Photosynthesis

来  源:   DOI:10.1128/aem.00863-24   PDF(Pubmed)

Abstract:
Purple sulfur bacteria (PSB) are capable of anoxygenic photosynthesis via oxidizing reduced sulfur compounds and are considered key drivers of the sulfur cycle in a range of anoxic environments. In this study, we show that Allochromatium vinosum (a PSB species) is capable of autotrophic growth using pyrite as the electron and sulfur source. Comparative growth profile, substrate characterization, and transcriptomic sequencing data provided valuable insight into the molecular mechanisms underlying the bacterial utilization of pyrite and autotrophic growth. Specifically, the pyrite-supported cell cultures (\"py\"\') demonstrated robust but much slower growth rates and distinct patterns from their sodium sulfide-amended positive controls. Up to ~200-fold upregulation of genes encoding various c- and b-type cytochromes was observed in \"py,\" pointing to the high relevance of these molecules in scavenging and relaying electrons from pyrite to cytoplasmic metabolisms. Conversely, extensive downregulation of genes related to LH and RC complex components indicates that the electron source may have direct control over the bacterial cells\' photosynthetic activity. In terms of sulfur metabolism, genes encoding periplasmic or membrane-bound proteins (e.g., FccAB and SoxYZ) were largely upregulated, whereas those encoding cytoplasmic proteins (e.g., Dsr and Apr groups) are extensively suppressed. Other notable differentially expressed genes are related to flagella/fimbriae/pilin(+), metal efflux(+), ferrienterochelin(-), and [NiFe] hydrogenases(+). Characterization of the biologically reacted pyrite indicates the presence of polymeric sulfur. These results have, for the first time, put the interplay of PSB and transition metal sulfide chemistry under the spotlight, with the potential to advance multiple fields, including metal and sulfur biogeochemistry, bacterial extracellular electron transfer, and artificial photosynthesis.
OBJECTIVE: Microbial utilization of solid-phase substrates constitutes a critical area of focus in environmental microbiology, offering valuable insights into microbial metabolic processes and adaptability. Recent advancements in this field have profoundly deepened our knowledge of microbial physiology pertinent to these scenarios and spurred innovations in biosynthesis and energy production. Furthermore, research into interactions between microbes and solid-phase substrates has directly linked microbial activities to the surrounding mineralogical environments, thereby enhancing our understanding of the relevant biogeochemical cycles. Our study represents a significant step forward in this field by demonstrating, for the first time, the autotrophic growth of purple sulfur bacteria using insoluble pyrite (FeS2) as both the electron and sulfur source. The presented comparative growth profiles, substrate characterizations, and transcriptomic sequencing data shed light on the relationships between electron donor types, photosynthetic reaction center activities, and potential extracellular electron transfer in these organisms capable of anoxygenic photosynthesis. Furthermore, the findings of our study may provide new insights into early-Earth biogeochemical evolutions, offering valuable constraints for understanding the environmental conditions and microbial processes that shaped our planet\'s history.
摘要:
紫色硫细菌(PSB)能够通过氧化还原的硫化合物进行缺氧光合作用,并被认为是一系列缺氧环境中硫循环的关键驱动因素。在这项研究中,我们表明,使用黄铁矿作为电子和硫源,长春变色菌(一种PSB物种)能够自养生长。比较生长概况,底物表征,和转录组测序数据为细菌利用黄铁矿和自养生长的分子机制提供了有价值的见解。具体来说,黄铁矿支持的细胞培养物(\“py\”\')表现出强劲但缓慢的生长速度和与硫化钠修正的阳性对照不同的模式。在py中观察到编码各种c型和b型细胞色素的基因上调约200倍,“指出这些分子在清除和传递电子从黄铁矿到细胞质代谢中的高度相关性。相反,与LH和RC复杂成分相关的基因的广泛下调表明电子源可能直接控制细菌细胞的光合活性。在硫代谢方面,编码周质或膜结合蛋白的基因(例如,FccAB和SoxYZ)在很大程度上上调,而那些编码细胞质蛋白(例如,Dsr和Apr组)被广泛抑制。其他值得注意的差异表达基因与鞭毛/菌毛/菌毛(+)有关,金属流出(+),ferrienterochelin(-),和[NiFe]氢化酶(+)。生物反应的黄铁矿的表征表明存在聚合硫。这些结果,第一次,把PSB和过渡金属硫化物化学的相互作用放在聚光灯下,具有推进多个领域的潜力,包括金属和硫生物地球化学,细菌胞外电子转移,和人工光合作用。
目的:固相基质的微生物利用构成了环境微生物学的关键领域,为微生物代谢过程和适应性提供有价值的见解。该领域的最新进展深刻加深了我们对与这些情景相关的微生物生理学的了解,并刺激了生物合成和能源生产方面的创新。此外,对微生物和固相基质之间相互作用的研究直接将微生物活动与周围的矿物学环境联系起来,从而增强我们对相关生物地球化学循环的理解。我们的研究表明,在这一领域向前迈出了重要的一步,第一次,使用不溶性黄铁矿(FeS2)作为电子和硫源的紫色硫细菌的自养生长。呈现的比较增长概况,底物表征,转录组测序数据揭示了电子供体类型之间的关系,光合反应中心活动,以及这些能够进行缺氧光合作用的生物体中潜在的细胞外电子转移。此外,我们的研究结果可能为早期地球生物地球化学演化提供新的见解,为理解塑造我们星球历史的环境条件和微生物过程提供了有价值的约束。
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