Microbial uptake dynamics of choline and glycine betaine in coastal seawater

Abstract

Choline and glycine betaine (GBT) are utilized as osmolytes to counteract osmotic stress, but also constitute important nutrient sources for many marine microbes. Bacterial catabolism of these substrates can then lead to the production of climate active trace gases such as methylamine and methane. Using radiotracers, we investigated prokaryotic choline/GBT uptake and determined biotic and abiotic factors driving these processes in the Western English Channel, UK. Kinetic uptake parameters indicated high affinity (nM range) for both osmolytes and showed a seasonal pattern for choline uptake. Generalized linear modeling of uptake parameters suggested a significant influence of sea surface temperature and salinity on prokaryotic uptake of both osmolytes. The presence of diatoms significantly influenced prokaryotic choline/GBT uptake dynamics. Choline uptake was further related to the occurrence of Phaeocystis spp., which were highly abundant in the phytoplankton community during spring, and dinoflagellates abundance during summer. While Rhodobacteraceae were the most important bacterial drivers for prokaryotic choline uptake, prokaryotic GBT uptake was associated with various groups such as SAR11 (Pelagibacterales) and Gammaproteobacteria, suggesting a wider capacity for GBT catabolism than previously recognized. Furthermore, using a newly developed approach we determined the first available data for dissolved GBT concentrations in seawater and found both osmolytes to be at the sub‐nanomolar range. Together, this study improves our understanding of the biogeochemical cycling of these environmentally important osmolytes and highlights how their cycles may be affected by a changing climate.

Bacterial catabolism of membrane phospholipids links marine biogeochemical cycles

“…While homologs of betT are also abundant and highly expressed, with maximal expression in mesopelagic waters, this BCCT-type transporter is usually nonspecific for various osmolytes, and caution regarding the importance of PC and choline in open ocean waters should be taken ( 31 , 52 ). choX is much more selective for choline, and the expression profile of this transporter supports our previous work ( 31 ), demonstrating that choline metabolism is restricted to bacteria typically associated with eukaryotic phytoplankton blooms in coastal region ( 55 ). Unlike that observed for the highly expressed tmoX and the less abundant choX (fig.…”

Quantification of dissolved metabolites in environmental samples through cation‐exchange solid‐phase extraction paired with liquid chromatography–mass spectrometry

“…The concentrations of many of the compounds measured in environmental samples by CX-SPE analysis are within or close to the environmental concentration ranges reported by other studies of dissolved metabolites such as amino acids (Lee and Bada 1975;Fuhrman and Ferguson 1986;Sabadel et al 2017), TMAO (Gibb and Hatton 2004), creatine (Wawrik et al 2017), DMSP (Kiene and Slezak 2006), and arsenobetaine (Glabonjat et al 2018) (Table 1). Furthermore, the concentrations of some compounds measured for the first time using CX-SPE such as glycine betaine were of roughly the same order of magnitude (low nM) as those predicted by uptake kinetics studies (Kiene and Slezak 2006;Boysen et al 2022;Mausz et al 2022). The overall composition of the compounds in the environmental samples fit our expectations based on observed particulate metabolite pools, with the most abundant particulate metabolites also contributing significantly to the quantifiable dissolved metabolite pool.…”

“…For example, glycine betaine and TMAO are key molecules in marine ecosystems that serve as osmolytes for marine microbes and animals (Welsh 2000;Yancey et al 2014), fixed C and N sources to marine microbes (Welsh 2000;Lidbury et al 2014;Boysen et al 2022), or precursors of methane and atmospheric aerosols (Lidbury et al 2015;Jones et al 2019). Until now, studies of these molecules have been restricted to the particulate phase (Heal et al 2021), molecular biology techniques (Ngugi et al 2020), indirect approximations through uptake kinetics studies (Boysen et al 2022;Mausz et al 2022), or a single, very targeted set of measurements (Gibb and Hatton 2004). CX-SPE enables some of the first measurements of these molecules, paving the way for future studies in understanding the distribution and cycling of these compounds.…”

Glycine betaine uptake and metabolism in marine microbial communities

“…GBT comprises a significant portion of intracellular metabolites in the North Pacific subtropical gyre and in the North Pacific transition zone (NPTZ) (Heal et al ., 2021) and exhibits diel oscillations indicative of active production and consumption (Boysen et al ., 2021). Incubation experiments with 14 C‐GBT show that natural microbial communities both respire and assimilate carbon from GBT (Kiene et al ., 1998; Kiene and Williams, 1998; Mausz et al ., 2022). However, GBT has complex biochemical potential, and previous work has left the flow and fate for GBT‐derived carbon and nitrogen mostly unresolved.…”