Sorokin Dimitry Y, Merkel Alexander Y, Ziganshin Rustam H, Kublanov Ilya V
Winogradsky Institute of Microbiology, Federal Research Centre of Biotechnology, Russian Academy of Sciences, Moscow, Russia.
Department of Biotechnology, Delft University of Technology, Delft, Netherlands.
Front Microbiol. 2025 May 23;16:1590477. doi: 10.3389/fmicb.2025.1590477. eCollection 2025.
Elemental sulfur disproportionation combined with obligate autotrophy is a unique type of sulfur-based anaerobic metabolism known in a limited number of bacteria, primarily found among the members of phylum. Until recently, the only characterized alkaliphilic representative of this group was , originally isolated as an H-dependent sulfur reducer. In this study, we describe the properties of a novel species within this genus, strain AMeS2, which was originally enriched and isolated from a soda lake sample as an autotrophic elemental sulfur disproportionating bacterium. Similar to AHT 2, AMeS2 is an obligately alkaliphilic and moderately salt-tolerant autotrophic bacterium. In contrast to known neutrophilic sulfur disproportionating bacteria, it is capable of disproportionating sulfur without Fe(III). It can also grow by dissimilatory sulfur reduction to sulfide or nitrate reduction to ammonium (DNRA) with formate (but not with H) as the electron donor. The addition of formate to sulfur-disproportionating AMeS2 culture significantly increased the sulfur-reducing activity but did not completely abolish the oxidative branch of sulfur disproportionation. Genome analysis confirmed the presence of dissimilatory sulfur oxidation and dissimilatory sulfur and nitrate reduction machineries in the strain. S disproportionation occurs by means of cytoplasmic dissimilatory sulfite reductase (Dsr) donating electrons to, and periplasmic polysulfide reductase (PsrABC) receiving electrons from the menaquinone pool. Nitrate reduction to ammonium (DNRA) occurs by the combined action of a membrane formate dehydrogenase FdnGHI, periplasmic nitrate reductase, and octaheme ammonifying nitrite reductase. Autotrophic growth is enabled by the Wood-Ljungdahl pathway (WLP). The genome also encodes proteins that presumably connect the oxidative branch of sulfur disproportionation with the carbon (WLP) cycle. Comparative proteomics of cells grown by sulfur disproportionation and formate-dependent DNRA demonstrated overexpression of the genes encoding Psr and rDSR at sulfur-disproportionating conditions, confirming their key role in this process. On the contrary, the genes encoding DNRA proteins are upregulated in the presence of nitrate. Thus, genomic and proteomic analyses revealed the pathways for energy conservation in a new representative of growing at DNRA and under the thermodynamically challenging conditions of sulfur disproportionation.
元素硫歧化作用与专性自养相结合是一种独特的基于硫的厌氧代谢类型，已知存在于少数细菌中，主要发现于某一门的成员中。直到最近，该类群中唯一被表征的嗜碱代表菌株是最初作为依赖氢的硫还原菌分离出来的。在本研究中，我们描述了该属内一个新物种菌株AME S2的特性，它最初是从一个苏打湖样品中富集并分离出来的自养元素硫歧化细菌。与菌株AHT 2相似，AME S2是一种专性嗜碱且耐盐适度的自养细菌。与已知的嗜中性硫歧化细菌不同，它能够在没有Fe(III)的情况下歧化硫。它还可以通过以甲酸盐（但不是氢）作为电子供体将硫异化还原为硫化物或将硝酸盐还原为铵（DNRA）来生长。向硫歧化的AME S2培养物中添加甲酸盐显著提高了硫还原活性，但并未完全消除硫歧化的氧化分支。基因组分析证实该菌株中存在异化硫氧化以及异化硫和硝酸盐还原机制。硫歧化通过细胞质异化亚硫酸盐还原酶（Dsr）向甲萘醌池提供电子以及周质多硫化物还原酶（PsrABC）从甲萘醌池接收电子来发生。硝酸盐还原为铵（DNRA）通过膜甲酸盐脱氢酶FdnGHI、周质硝酸盐还原酶和八血红素氨化亚硝酸盐还原酶的联合作用来发生。自养生长通过伍德-Ljungdahl途径（WLP）实现。该基因组还编码可能将硫歧化的氧化分支与碳（WLP）循环连接起来的蛋白质。对通过硫歧化和依赖甲酸盐的DNRA生长的细胞进行的比较蛋白质组学研究表明，在硫歧化条件下，编码Psr和rDSR的基因过表达，证实了它们在这一过程中的关键作用。相反，编码DNRA蛋白的基因在有硝酸盐存在时上调。因此，基因组和蛋白质组分析揭示了在DNRA条件下以及在硫歧化的热力学挑战性条件下生长的该属新代表菌株中的能量守恒途径。
