Different Bacterial Communities Involved in Peptide Decomposition between Normoxic and Hypoxic Coastal Waters

Abstract

Proteins and peptides are key components of the labile dissolved organic matter pool in marine environments. Knowing which types of bacteria metabolize peptides can inform the factors that govern peptide decomposition and further carbon and nitrogen remineralization in marine environments. A 13C-labeled tetrapeptide, alanine-valine-phenylalanine-alanine (AVFA), was added to both surface (normoxic) and bottom (hypoxic) seawater from a coastal station in the northern Gulf of Mexico for a 2-day incubation experiment, and bacteria that incorporated the peptide were identified using DNA stable isotope probing (SIP). The decomposition rate of AVFA in the bottom hypoxic seawater (0.018–0.035 μM h-1) was twice as fast as that in the surface normoxic seawater (0.011–0.017 μM h-1). SIP experiments indicated that incorporation of 13C was highest among the Flavobacteria, Sphingobacteria, Alphaproteobacteria, Acidimicrobiia, Verrucomicrobiae, Cyanobacteria, and Actinobacteria in surface waters. In contrast, highest 13C-enrichment was mainly observed in several Alphaproteobacteria (Thalassococcus, Rhodobacteraceae, Ruegeria) and Gammaproteobacteria genera (Colwellia, Balneatrix, Thalassomonas) in the bottom water. These data suggest that a more diverse group of both oligotrophic and copiotrophic bacteria may be involved in metabolizing labile organic matter such as peptides in normoxic coastal waters, and several copiotrophic genera belonging to Alphaproteobacteria and Gammaproteobacteria and known to be widely distributed may contribute to faster peptide decomposition in the hypoxic waters.

Distinct capabilities of different Gammaproteobacterial strains on utilizing small peptides in seawater

“…As there is ecological difference among bacterial strains even within the same species 96 , we used four Gammaproteobacterial strains as models for their corresponding bacterial species to demonstrate their potential capability of peptide decomposition. The rapid responses of these bacterial strains (Pseudoalteromonas and Alteromonas) to peptides are consistent to field studies of peptide decomposition using natural bacterial assemblages containing these species 16,25,43 , indicating our chosen bacterial strains can represent in some degree their corresponding species in peptide decomposition. In contrast, while Marinobacterium and Amphritea showed rapid increase in natural assemblages when incubated with AVFA 16,45 , they did not grow as single strain incubations, indicating they were using byproducts from AVFA decomposition by other bacteria in natural assemblages.…”

“…The evolving dominance of certain bacterial taxa with incubation time implies that different bacterial taxa may have different capabilities on decomposition of labile DOM, and certain copiotrophic bacteria may metabolize the substrate faster than others. Through the techniques of Microautoradiography-Fluorescent in situ hybridization (MAR-FISH) and stable isotope probing (SIP), it is identified that Alphaproteobacteria such as Rhodobacterales and Ruegeria, Gammaproteobacteria such as Alteromonas, and Flavobacterium group efficiently take up labile organic matter including peptides, proteins, amino acids or sugars in natural waters, further indicating their outstanding capability of labile substrate utilization [22][23][24][25] .…”

“…Even though a tight relationship between bacterial communities and peptide decomposition has been suggested 25 , direct evidence of whether different bacteria differ in their peptide decomposition capabilities is lacking. Protein decomposition in single bacterial strain cultures has been studied [38][39][40] , but small peptide decomposition has not been well-explored.…”

“…To better understand capabilities of different bacteria on peptide decomposition, we incubated a model tetrapeptide, alanine-valine-phenylalanine-alanine (AVFA), with four individual Gammaproteobacterial strains, including Pseudoalteromonas atlantica, Alteromonas sp., Marinobacterium jannaschii, and Amphritea japonica. AVFA is a fragment of ribulose-1,5-biphosphate carboxylase/oxygenase (RuBisCO) that is ubiquitously involved in photosynthesis, and has been applied in our previous peptide decomposition studies 16,25 . These four bacterial strains were chosen because their growth has been often observed in substrate addition incubations in coastal waters [41][42][43][44][45] 100 fold change of relative abundance from amplicon sequencing, Table 1).…”

Prokaryotic niche partitioning between suspended and sinking marine particles

“…In the upper-mesopelagic, sinking particle-associated communities were significantly enriched with Gammaproteobacteria (including Pseudomonadales, Vibrionales and Pasteurellales), Alphaproteobacteria (Rhodobacterales and Rhizobiales), Actinobacteria and Firmicutes. Gammaproteobacterial Pseudomonadales and Vibrionales (Pinhassi and Berman, 2003;Allers et al, 2007;Mason et al, 2012;Stewart et al, 2012;Logue et al, 2016;Liu et al, 2017), as well as members of Rhodobacterales, including Rhodobacteraceae (Buchan et al, 2005;Brinkhoff et al, 2008;Mayali et al, 2015), are generalist copiotrophs exhibiting surface-attachment capabilities (e.g., biofilm formation, pili, non-specific extracellular polymers and proteins). Their versatile metabolic capabilities allow them to utilise a wide spectrum of phytoplankton-derived organic matter substrates, ranging from monocyclic to aromatic compounds (labile to more refractory compounds) (Sperling et al, 2017).…”