Hogle Shane L, Brahamsha Bianca, Barbeau Katherine A
Geosciences Research Division, Scripps Institution of Oceanography, La Jolla, California, USA.
Marine Biology Research Division, Scripps Institution of Oceanography, La Jolla, California, USA.
mSystems. 2017 Jan 10;2(1). doi: 10.1128/mSystems.00124-16. eCollection 2017 Jan-Feb.
Iron is an essential micronutrient and can limit the growth of both marine phytoplankton and heterotrophic bacterioplankton. In this study, we investigated the molecular basis of heme transport, an organic iron acquisition pathway, in phytoplankton-associated bacteria and explored the potential role of bacterial heme uptake in the marine environment. We searched 153 genomes and found that nearly half contained putative complete heme transport systems with nearly the same synteny. We also examined a publicly available coculture transcriptome and found that strain sp. strain SA11 strongly downregulated a putative heme transport gene cluster during mutualistic growth with a marine diatom, suggesting that the regulation of heme transport might be influenced by host cues. We generated a mutant of phytoplankton-associated strain Ruegeria sp. strain TM1040 by insertionally inactivating its homolog of the TonB-dependent heme transporter and confirmed the role of this gene in the uptake of heme and hemoproteins. We performed competition experiments between iron-limited wild-type and mutant TM1040 strains and found that the wild type maintains a growth advantage when competing with the mutant for iron compounds derived solely from lysed diatom cells. Heme transport systems were largely absent from public marine metagenomes and metatranscriptomes, suggesting that marine bacteria with the potential for heme transport likely have small standing populations in the free-living bacterioplankton. Heme transport is likely a useful strategy for phytoplankton-associated bacteria because it provides direct access to components of the host intracellular iron pool after lysis. Ecosystem productivity in large regions of the surface ocean is fueled by iron that has been microbially regenerated from biomass. Currently, the specific microbes and molecules that mediate the transfer of recycled iron between microbial trophic levels remain largely unknown. We characterized a marine bacterial heme transporter and verified its role in acquiring heme, an abundant iron-containing enzyme cofactor. We present evidence that after host cell lysis, phytoplankton-associated bacteria directly extract heme and hemoproteins from algal cellular debris in order to fulfill their iron requirements and that the regulation of this process may be modulated by host cues. Direct heme transport, in contrast to multistep extracellular processing of hemoproteins, may allow certain phytoplankton-associated bacteria to rapidly extract iron from decaying phytoplankton, thus efficiently recycling cellular iron into the wider microbial loop.
铁是一种必需的微量营养素，它能够限制海洋浮游植物和异养浮游细菌的生长。在本研究中，我们调查了浮游植物相关细菌中血红素转运（一种有机铁获取途径）的分子基础，并探讨了细菌血红素摄取在海洋环境中的潜在作用。我们搜索了153个基因组，发现近一半基因组含有具有几乎相同同线性的假定完整血红素转运系统。我们还研究了一个公开的共培养转录组，发现菌株sp. 菌株SA11在与海洋硅藻共生生长期间强烈下调了一个假定的血红素转运基因簇，这表明血红素转运的调控可能受到宿主信号的影响。我们通过插入失活其与TonB依赖性血红素转运蛋白同源的基因，构建了浮游植物相关菌株鲁杰氏菌属sp. 菌株TM1040的突变体，并证实了该基因在血红素和血红蛋白摄取中的作用。我们对铁限制的野生型和突变体TM1040菌株进行了竞争实验，发现野生型在与突变体竞争仅来自裂解硅藻细胞的铁化合物时保持生长优势。公共海洋宏基因组和宏转录组中基本上不存在血红素转运系统，这表明具有血红素转运潜力的海洋细菌在自由生活的浮游细菌中可能具有较小的现存种群。血红素转运可能是浮游植物相关细菌的一种有用策略，因为它在宿主细胞裂解后能够直接获取宿主细胞内铁库的成分。表层海洋大片区域的生态系统生产力是由从生物量中微生物再生的铁所推动的。目前，介导微生物营养级之间循环铁转移的具体微生物和分子在很大程度上仍然未知。我们对一种海洋细菌血红素转运蛋白进行了表征，并证实了其在获取血红素（一种丰富的含铁酶辅因子）中的作用。我们提供的证据表明，宿主细胞裂解后，浮游植物相关细菌直接从藻类细胞碎片中提取血红素和血红蛋白以满足其铁需求，并且这一过程的调控可能受到宿主信号的调节。与血红蛋白的多步细胞外加工相反，直接血红素转运可能使某些浮游植物相关细菌能够从腐烂的浮游植物中快速提取铁，从而有效地将细胞内铁循环到更广泛的微生物环中。
