Interkingdom Cross-Feeding of Ammonium from Marine Methylamine-Degrading Bacteria to the Diatom Phaeodactylum tricornutum
Interkingdom Cross-Feeding of Ammonium from Marine Methylamine-Degrading Bacteria to the Diatom Phaeodactylum tricornutum
复制标题
DOI：
10.1128/aem.01642-16
复制
发表时间：
2016-09
影响因子：
4.4
通讯作者：
Marcel Suleiman;Karsten Zecher;O. Yücel;Nina Jagmann;B. Philipp
中科院分区：
文献类型：
--
作者：
Marcel Suleiman;Karsten Zecher;O. Yücel;Nina Jagmann;B. Philipp
摘要甲胺广泛存在于海洋中，可以作为海洋浮游细菌中不同系统发育类群的异养细菌的碳源、氮源和能源。硅藻是海洋浮游植物中的重要组成部分，据信它们不能利用甲胺作为氮源。由于硅藻通常与异养细菌相关联，因此提出了甲基营养细菌可能通过降解甲胺为硅藻提供铵的假设。以三角褐指藻和一甲胺（MMA）为底物研究了这一假说。从海水中分离得到了以甲基丙烯酸甲酯为唯一氮源的三角褐指藻光合自养生长支持菌。选择了两种菌株，即具有单甲胺脱氢酶和N-甲基谷氨酸途径基因的Donghicola sp.菌株KarMa和通过MMA脱氢酶催化MMA氧化的Methylophaga sp.菌株M1，用于进一步表征。虽然菌株M1以MMA作为唯一底物生长，但菌株KarMa仅在以下情况下才能利用MMA作为氮源，例如，提供葡萄糖作为碳源。与这两种菌株，释放的铵在MMA利用过程中检测。在与三角褐指藻的共培养中，KarMa菌株与2 mM MMA一起支持光合自养生长，其程度与等摩尔量的NH 4Cl相同。在与菌株M1共培养时，三角褐指藻的光合自养生长也得到了支持，但支持程度远低于菌株KarMa。这证明了原理的研究与合成的微生物群落表明，跨王国交叉喂养的铵从甲胺降解细菌是浮游植物的生长，这一直被忽视到目前为止的贡献。硅藻和异养细菌之间的相互作用对海洋碳循环非常重要。在这项研究中，描述了一种新的相互作用。一甲胺是海洋环境中普遍存在的有机氮化合物，能够降解一甲胺的细菌可以为硅藻提供铵。这种界间代谢物的转移使得在共培养的光合自养条件下能够生长，这在各自的单一培养中是不可能的。这项原理验证研究引起了人们对迄今为止被忽视的浮游植物生长的关注。
ABSTRACT Methylamines occur ubiquitously in the oceans and can serve as carbon, nitrogen, and energy sources for heterotrophic bacteria from different phylogenetic groups within the marine bacterioplankton. Diatoms, which constitute a large part of the marine phytoplankton, are believed to be incapable of using methylamines as a nitrogen source. As diatoms are typically associated with heterotrophic bacteria, the hypothesis came up that methylotrophic bacteria may provide ammonium to diatoms by degradation of methylamines. This hypothesis was investigated with the diatom Phaeodactylum tricornutum and monomethylamine (MMA) as the substrate. Bacteria supporting photoautotrophic growth of P. tricornutum with MMA as the sole nitrogen source could readily be isolated from seawater. Two strains, Donghicola sp. strain KarMa, which harbored genes for both monomethylamine dehydrogenase and the N methylglutamate pathway, and Methylophaga sp. strain M1, which catalyzed MMA oxidation by MMA dehydrogenase, were selected for further characterization. While strain M1 grew with MMA as the sole substrate, strain KarMa could utilize MMA as a nitrogen source only when, e.g., glucose was provided as a carbon source. With both strains, release of ammonium was detected during MMA utilization. In coculture with P. tricornutum, strain KarMa supported photoautotrophic growth with 2 mM MMA to the same extent as with the equimolar amount of NH4Cl. In coculture with strain M1, photoautotrophic growth of P. tricornutum was also supported, but to a much lower degree than by strain KarMa. This proof-of-principle study with a synthetic microbial community suggests that interkingdom cross-feeding of ammonium from methylamine-degrading bacteria is a contribution to phytoplankton growth which has been overlooked so far. IMPORTANCE Interactions between diatoms and heterotrophic bacteria are important for marine carbon cycling. In this study, a novel interaction is described. Bacteria able to degrade monomethylamine, which is a ubiquitous organic nitrogen compound in marine environments, can provide ammonium to diatoms. This interkingdom metabolite transfer enables growth under photoautotrophic conditions in coculture, which would not be possible in the respective monocultures. This proof-of-principle study calls attention to a so far overlooked contribution to phytoplankton growth.