Occurrence and degradation of peptidoglycan in aquatic environments

Abstract

Mechanisms controlling microbial degradation of dissolved organic matter (DOM) in aquatic environments are poorly understood, although microbes are crucial to global nutrient cycling. Bacterial cell wall components may be one of the keys in understanding the presence of slowly degrading DOM in nature. We found that dominant components of bacterial cell walls (D-amino acids (D-AA), glucosamine (GluA) and diaminopimelic acid (DAPA)) comprised up to 11.4% of the dissolved organic nitrogen in 50 diverse rivers entering the Baltic Sea. Occurrence of DAPA, a characteristic component of Gram-negative (G(-)) bacteria, in the rivers suggests that G(-) bacteria rather than Gram-positive (G(+)) were the major source of the cell wall material. In laboratory studies, the degradation of whole bacterial cells, cell wall material and purified peptidoglycan was studied to characterize degradation of cell wall material by natural aquatic bacteria. Addition of whole killed G(-) and G(+) bacteria to cultures of estuarine bacteria demonstrated fragmentation and loss of cell structure of the G(+) bacteria, while the G(-) bacteria maintained an intact cell shape during the entire 69-day period. In another experiment, estuarine bacteria degraded 39-69% of GluA, D-AA and DAPA in added cell wall material of a representative G(-) bacterial species during 8 days, as compared to a 72-89% degradation of GluA, D-AA and DAPA in cell material of a G(+) bacterial species. When cultures of estuarine bacteria were enriched with purified G(-) and G(+) peptidoglycan (1 mg l(-1)), at least 49% (G(-)) and 58% (G(+)) of D-AA in the peptidoglycan was degraded. No major changes in GluA were obvious. Interpretation of the results was difficult as a portion of the purified peptidoglycan was of similar size to the bacteria and could not be differentiated from cells growing in the cultures. Addition of the purified peptidoglycan stimulated the bacterial growth, and after 6 days the cell density in the enriched cultures was 4-fold higher than in the controls. A regrowth of bacteria after addition of L-broth at 105 days caused a 50- to 75-fold increase in dissolved D-AA and GluA. Most of the D-AA and GluA were taken up during the following 10 days, indicating that cell wall constituents are dynamic compounds. Our results show that a variable portion of peptidoglycan in G(-) and G(+) bacteria can be degraded by natural bacteria, and that peptidoglycan in G(-) bacteria is more resistant to bacterial attack than that in G(+) bacteria. Thus, the presence of cell wall constituents in natural DOM may reflect the recalcitrant nature of especially G(-) peptidoglycan.

Phage infection of an environmentally relevant marine bacterium alters host metabolism and lysate composition

“…Metabolites with increased relative concentrations in the filtrates were those typically related to cellular stress or those that are potentially too large to be transported into the cell (that is, 4600 Da; Benz, 1985;Williams, 2000). The presence of bacterial cell wall constituents (that is, phosphatidylcholine and phosphatidylethanolamine) in the phage-infected culture filtrates is also consistent with the degradation of cell wall material from lysed cells and with prior studies demonstrating the prevalence and recalcitrance of bacterial cell wall components (that is, peptidoglycan) in marine (McCarthy et al, 1998;Pedersen et al, 2001;Jørgensen et al, 2003) and virus-derived DOM (Middelboe and Jorgensen, 2006). Dissolved and free amino acids have also been previously identified in viral lysates (Middelboe and Jorgensen, 2006), but the contribution of individual amino acids was not reported.…”

Fate of peptidoglycan in an intertidal sediment: An in situ 13C‐labeling study

“…This relatively strong retention of D-Ala (i.e., peptidoglycan) is consistent with the relatively low degradability of peptidoglycan in laboratory experiments (Jørgensen et al 2003;Nagata et al 2003). Hence, results show that the potential for accumulation of peptidoglycan is also present during reworking and degradation of bacterial biomass in the highly dynamic upper centimeters of an intertidal sediment.…”

Sources, distributions, and early diagenesis of sedimentary organic matter in the Pearl River region of the South China Sea

“…DAPA is a unique amino acid that is found in the cell wall polymer, peptidoglycan, of Gram negative bacteria (Jørgensen et al, 2003). The occurrence of DAPA in marine sediments is indicative of both living bacteria and remnants of bacterial cells (Lomstein et al, 2009).…”