Metatranscriptomic Evidence for Direct Interspecies Electron Transfer between Geobacter and Methanothrix Species in Methanogenic Rice Paddy Soils
Metatranscriptomic Evidence for Direct Interspecies Electron Transfer between Geobacter and Methanothrix Species in Methanogenic Rice Paddy Soils
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DOI：
10.1128/aem.00223-17
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发表时间：
2017-05-01
影响因子：
4.4
通讯作者：
Lovley, Derek R.
中科院分区：
文献类型：
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作者：
Holmes, Dawn E.;Shrestha, Pravin M.;Lovley, Derek R.
在稻田土壤中研究了甲烷丝菌（以前称为甲烷菌）和地杆菌属在陆地产甲烷环境中通过直接种间电子转移（DIET）进行合作的可能性。与硫还原地杆菌导电菌毛（e-pili）的 PilA 菌毛单体基因具有高度序列相似性的基因占宏基因组文库中 PilA 基因序列的一半以上，占 RNA 测序（RNA-seq）文库中 mRNA 转录本的 42%。如此丰富的 e-pilin 基因和转录本非常重要，因为 e-pilin 可以作为 DIET 的管道。大多数 e-pilin 基因和转录本属于地杆菌属物种，但也检测到了与脱硫杆菌属、去铁杆菌属、地碱杆菌属和脱硫杆菌属等推定的 e-pilin 基因最密切相关的序列。大约 17% 的宏基因组和宏转录组细菌序列与 Geobacter 物种聚集在一起，并且发现 Geobacter spp。积极转录与生长相关的基因表明它们在土壤中代谢活跃。编码 e-pilin 的基因是转录程度最高的地杆菌基因之一。此外，编码 OmcS 的基因的同源物也在土壤中高度表达，OmcS 是一种与 G.sulfurreducens 的 e-菌毛相关的 c 型细胞色素，并且是 DIET 所需的。土壤中的甲烷丝菌高度表达参与将二氧化碳还原为甲烷的酶基因。 DIET 是已知唯一支持甲烷丝菌 CO2 还原的电子供体。因此，这些结果与地杆菌属物种通过电子菌毛的电连接向甲烷丝菌属物种提供电子以产生甲烷的模型是一致的。 重要性 甲烷丝菌属物种是全球甲烷生产最重要的微生物贡献者之一，但令人惊讶的是，人们对其生理学和生态学知之甚少。 DIET 是产甲烷稻田土壤中甲烷丝菌的电子源的可能性很重要，因为它表明甲烷丝菌对陆地环境中甲烷产生的贡献可能超出了乙酸盐转化为甲烷的范围。此外，明确的共培养研究表明，当甲烷丝菌物种从饮食中获取部分能量时，它们的生长速度比醋酸盐作为其唯一能源时生长得更快。因此，甲烷丝菌在产甲烷土壤中的生长和代谢可能比通常认为的更快、更强劲。研究结果还表明，地杆菌属物种多次被发现是产甲烷土壤中代谢最活跃的微生物之一的原因是它们通过饮食与甲烷丝菌属以及可能的其他产甲烷菌协同生长。
The possibility that Methanothrix (formerly Methanosaeta) and Geobacter species cooperate via direct interspecies electron transfer (DIET) in terrestrial methanogenic environments was investigated in rice paddy soils. Genes with high sequence similarity to the gene for the PilA pilin monomer of the electrically conductive pili (e-pili) of Geobacter sulfurreducens accounted for over half of the PilA gene sequences in metagenomic libraries and 42% of the mRNA transcripts in RNA sequencing (RNA-seq) libraries. This abundance of e-pilin genes and transcripts is significant because e-pili can serve as conduits for DIET. Most of the e-pilin genes and transcripts were affiliated with Geobacter species, but sequences most closely related to putative e-pilin genes from genera such as Desulfobacterium, Deferribacter, Geoalkalibacter, and Desulfobacula, were also detected. Approximately 17% of all metagenomic and metatranscriptomic bacterial sequences clustered with Geobacter species, and the finding that Geobacter spp. were actively transcribing growth-related genes indicated that they were metabolically active in the soils. Genes coding for e-pilin were among the most highly transcribed Geobacter genes. In addition, homologs of genes encoding OmcS, a c-type cytochrome associated with the e-pili of G. sulfurreducens and required for DIET, were also highly expressed in the soils. Methanothrix species in the soils highly expressed genes for enzymes involved in the reduction of carbon dioxide to methane. DIET is the only electron donor known to support CO2 reduction in Methanothrix. Thus, these results are consistent with a model in which Geobacter species were providing electrons to Methanothrix species for methane production through electrical connections of e-pili.IMPORTANCE Methanothrix species are some of the most important microbial contributors to global methane production, but surprisingly little is known about their physiology and ecology. The possibility that DIET is a source of electrons for Methanothrix in methanogenic rice paddy soils is important because it demonstrates that the contribution that Methanothrix makes to methane production in terrestrial environments may extend beyond the conversion of acetate to methane. Furthermore, defined coculture studies have suggested that when Methanothrix species receive some of their energy from DIET, they grow faster than when acetate is their sole energy source. Thus, Methanothrix growth and metabolism in methanogenic soils may be faster and more robust than generally considered. The results also suggest that the reason that Geobacter species are repeatedly found to be among the most metabolically active microorganisms in methanogenic soils is that they grow syntrophically in cooperation with Methanothrix spp., and possibly other methanogens, via DIET.