Gao Chao, Zhang Nan, He Xiao-Yan, Wang Ning, Zhang Xi-Ying, Wang Peng, Chen Xiu-Lan, Zhang Yu-Zhong, Ding Jun-Mei, Li Chun-Yang
State Key Laboratory of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, China.
College of Marine Life Sciences, Frontiers Science Center for Deep Ocean Multispheres and Earth System, Ocean University of China, Qingdao, China.
Front Microbiol. 2022 Feb 28;13:838608. doi: 10.3389/fmicb.2022.838608. eCollection 2022.
Trimethylamine -oxide (TMAO), which was detected at nanomolar concentrations in surface seawaters, is an important carbon, nitrogen and/or energy source for marine bacteria. It can be metabolized by marine bacteria into volatile methylated amines, the second largest source of nitrogen after N gas in the oceans. The SAR11 bacteria are the most abundant oligotrophic plankton in the oceans, which represents approximately 30% of the bacterial cells in marine surface waters. Genomic analysis suggested that most SAR11 bacteria possess an ATP-binding cassette transporter TmoXWV that may be responsible for importing TMAO. However, it was still unclear whether SAR11 bacteria can utilize TMAO as the sole nitrogen source and how they import TMAO. Here, our results showed that strain HTCC1062, a SAR11 bacterium, can grow with TMAO as the sole nitrogen source. TmoXWV from strain HTCC1062 (TmoXWV) was verified to be a functional TMAO importer. Furthermore, TmoX, the periplasmic substrate binding protein of TmoXWV, was shown to have high binding affinities toward TMAO at 4°C ( = 920 nM), 10°C ( = 500 nM) and 25°C ( = 520 nM). The high TMAO binding affinity and strong temperature adaptability of TmoX reveal a possible oligotrophic niche adaptation strategy of strain HTCC1062, which may help it gain a competitive advantage over other bacteria. Structure comparison and mutational analysis indicated that the TMAO binding mechanism of TmoX may have differences from the previously reported mechanism of TmoX of DSS-3. This study provides new insight into TMAO utilization by the widespread SAR11 bacteria.
氧化三甲胺(TMAO)在表层海水中的浓度为纳摩尔级,它是海洋细菌重要的碳、氮和/或能量来源。海洋细菌可将其代谢为挥发性甲基化胺,这是海洋中仅次于氮气的第二大氮源。SAR11细菌是海洋中最丰富的贫营养浮游生物,约占海洋表层水体细菌细胞的30%。基因组分析表明,大多数SAR11细菌拥有一个ATP结合盒转运体TmoXWV,可能负责转运TMAO。然而,SAR11细菌是否能将TMAO作为唯一氮源以及它们如何转运TMAO仍不清楚。在此,我们的结果表明,SAR11细菌菌株HTCC1062能够以TMAO作为唯一氮源生长。来自菌株HTCC1062的TmoXWV(TmoXWV)被证实是一种功能性TMAO转运体。此外,TmoXWV的周质底物结合蛋白TmoX在4°C(Kd = 920 nM)、10°C(Kd = 500 nM)和25°C(Kd = 520 nM)时对TMAO具有高结合亲和力。TmoX对TMAO的高结合亲和力和强大的温度适应性揭示了菌株HTCC1062一种可能的贫营养生态位适应策略,这可能有助于它比其他细菌获得竞争优势。结构比较和突变分析表明,TmoX的TMAO结合机制可能与先前报道的DSS - 3的TmoX机制有所不同。本研究为广泛存在的SAR11细菌利用TMAO提供了新的见解。