Metatranscriptomic identification of polyamine‐transforming bacterioplankton in the Gulf of Mexico

Abstract

The importance of short-chained aliphatic polyamines (PAs) to bacterioplankton-mediated carbon and nitrogen cycles has been repeatedly proposed. However, bacterial taxa and genes involved in the transformations of different PA compounds and their potential spatial variations remain unclear. This study collected surface bacterioplankton from nearshore, offshore, and open ocean stations in the Gulf of Mexico and examined how metatranscriptomes responded to additions of three single PA model compounds (i.e. putrescine, spermidine, or spermine). Our data showed an overrepresentation of genes affiliated with γ-glutamylation and spermidine cleavage pathways in metatranscriptomes received PA amendments and the expression level of each pathway varied among different PA compounds and sampling locations. PA-transforming taxa were affiliated with Actinobacteria, Bacteroidetes, Cyanobacteria, Planctomycetes, and Proteobacteria and their relative importance was also compound and location specific. These findings suggest that PAs are transformed via multiple pathways and by a diversity of marine bacterioplankton in the Gulf of Mexico. The relative importance of different PA transforming pathways and composition of functional microbial communities may be regulated by nutrient status of local environments.

SAR11 Cells Rely on Enzyme Multifunctionality To Metabolize a Range of Polyamine Compounds

“…SPD metabolism has been observed in marine bacteria without a spermidine dehydrogenase gene ( spdH ) ( 9 , 11 , 28 ). It has been speculated that the enzyme that synthesizes SPD from PUT, SpeE, is bi-directional, although this activity was not confirmed experimentally ( 9 ), and SpeE is known to not be bi-directional in other cell types ( 44 , 45 ).…”

“…Putrescine (PUT) and spermidine (SPD), the most abundant polyamines in the oceanic dissolved pool, are typically 3 to 5 nM in the environment, but spermine, cadaverine (CAD), and norspermidine (NSD) have been detected at lower levels ( 6 , 10 , 11 ). Several other polyamines, such as 1,3-diaminopropane (DAP), agmatine (AGM), homospermidine (HSD), spermine, and larger, more complex polyamines are known to be produced and/or metabolized by cells from all domains of life ( 3 , 4 , 9 , 12 , 13 ).…”

SAR11 Cells Rely on Enzyme Multifunctionality to Transport and Metabolize a Range of Polyamine Compounds

“…SPD metabolism has been observed in marine bacteria without a spermidine dehydrogenase gene (spdH) (9,11,25). It has been speculated that the enzyme that synthesizes SPD from PUT, SpeE, is bi-directional, although this activity was not confirmed experimentally (9).…”

“…Putrescine (PUT) and spermidine (SPD), the most abundant polyamines in the ocean, are typically 3-5 nM in the environment, but spermine, cadaverine (CAD), and norspermidine (NSD) have been detected at lower levels (6,10,11). Several other polyamines, such as 1,3diaminopropane (DAP), agmatine (AGM), homospermidine (HSD), spermine, and larger, more complex polyamines are known to be produced and/or metabolized by cells from all domains of life (3,4,9,12,13).…”

Metagenomes of polyamine-transforming bacterioplankton along a nearshore–open ocean transect

“…A large number of studies on bacteria-mediated DON transformation have been focused on amino acids and urea. However, increasing attention has been given to a group of understudied DON compounds [i.e., polyamines (PAs)] (Liu et al 2015;Lu et al 2014Lu et al , 2020, which are produced by organisms of all three life domains (Tabor and Tabor 1984) and mediate a number of essential cellular functions Kashiwagi 1999, 2000). PAs share many biogeochemical features with amino acids, such as C:N ratio, wide distribution, and low concentrations (nmol/L level) in seawater (Lee and Jørgensen 1995;Lu et al 2014).…”