Interkingdom cross-feeding of ammonium from marine methylamine-degrading bacteria to the diatom Phaeodactylum tricornutum

Journal
Applied and environmental microbiology  
Volume
82
Issue
24
Start Page
7113
End Page
7122
Citation
Applied and Environmental Microbiology 24 (82): 7113-7122 (2016)
Publisher DOI
10.1128/AEM.01642-16
Scopus ID
2-s2.0-84997427339
Publisher
Soc.
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 catalyzedMMAoxidation byMMA dehydrogenase, were selected for further characterization. While strain M1 grew withMMAas the sole substrate, strain KarMa could utilizeMMAas 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 2mMMMAto 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 methylaminedegrading bacteria is a contribution to phytoplankton growth which has been overlooked so far.
DDC Class
570: Biowissenschaften, Biologie