scholarly journals Cooperation and spatial self-organization determine rate and efficiency of particulate organic matter degradation in marine bacteria

2019 ◽  
Vol 116 (46) ◽  
pp. 23309-23316 ◽  
Author(s):  
Ali Ebrahimi ◽  
Julia Schwartzman ◽  
Otto X. Cordero

The recycling of particulate organic matter (POM) by microbes is a key part of the global carbon cycle. This process is mediated by the extracellular hydrolysis of polysaccharides, which can trigger social behaviors in bacteria resulting from the production of public goods. Despite the potential importance of public good-mediated interactions, their relevance in the environment remains unclear. In this study, we developed a computational and experimental model system to address this challenge and studied how the POM depolymerization rate and its uptake efficiency (2 main ecosystem function parameters) depended on social interactions and spatial self-organization on particle surfaces. We found an emergent trade-off between rate and efficiency resulting from the competition between oligosaccharide diffusion and cellular uptake, with low rate and high efficiency being achieved through cell-to-cell cooperation between degraders. Bacteria cooperated by aggregating in cell clusters of ∼10 to 20 µm, in which cells were able to share public goods. This phenomenon, which was independent of any explicit group-level regulation, led to the emergence of critical cell concentrations below which degradation did not occur, despite all resources being available in excess. In contrast, when particles were labile and turnover rates were high, aggregation promoted competition and decreased the efficiency of carbon use. Our study shows how social interactions and cell aggregation determine the rate and efficiency of particulate carbon turnover in environmentally relevant scenarios.

2019 ◽  
Author(s):  
Ali Ebrahimi ◽  
Julia Schwartzman ◽  
Otto X. Cordero

AbstractThe recycling of particulate organic matter (POM) by microbes is a key part of the global carbon cycle, one which is mediated by the extracellular hydrolysis of polysaccharides and the production of public goods that can trigger social behaviors in bacteria. Despite the potential importance of these microbial interactions, their role in regulating of ecosystem function remains unclear. In this study, we developed a computational and experimental model system to address this challenge and studied how POM depolymerization rate and its uptake efficiency –two main ecosystem function parameters– depended on social interactions and spatial self-organization on particle surfaces. We found an emergent trade-off between rate and efficiency resulting from the competition between oligosaccharide diffusion and cellular uptake, with low rate and high efficiency being achieved through cell-to-cell cooperation between degraders. Bacteria cooperated by aggregating in cell-clusters of ~10-20μm, where cells were able to share public goods. This phenomenon, which was independent of any explicit group-level regulation, led to the emergence of critical cell concentrations below which degradation did not occur, despite all resources being available in excess. By contrast, when particles were labile and turnover rates were high, aggregation promoted competition and decreased the efficiency of carbon utilization. Our study shows how social interactions and cell aggregation determine the rate and efficiency of particulate carbon turnover in environmentally relevant scenarios.Significance StatementMicroorganisms can cooperate by secreting public goods that benefit local neighbors, however, the impact of cooperation on ecosystem functions remains poorly constrained. We here pair computation and experiment to show that bacterial cooperation mediates the degradation of polysaccharide particles recalcitrant to hydrolysis in aquatic environments. On particle surfaces, cooperation emerges through the self-organization of cells into ~10-20μm clusters that promote cooperative uptake of hydrolysis products. The transition between cooperation and competition in aggregates is mitigated by individual cell behaviors such as motility and chemotaxis, that promote reorganization on the particle surface. When cooperation is required, the degradation of recalcitrant biopolymers can only take place when degraders exceed a critical cell concentration, underscoring the importance of microbial interactions for ecosystem function.


1998 ◽  
Vol 38 (8-9) ◽  
pp. 179-188 ◽  
Author(s):  
K. F. Janning ◽  
X. Le Tallec ◽  
P. Harremoës

Hydrolysis and degradation of particulate organic matter has been isolated and investigated in laboratory scale and pilot scale biofilters. Wastewater was supplied to biofilm reactors in order to accumulate particulates from wastewater in the filter. When synthetic wastewater with no organic matter was supplied to the reactors, hydrolysis of the particulates was the only process occurring. Results from the laboratory scale experiments under aerobic conditions with pre-settled wastewater show that the initial removal rate is high: rV, O2 = 2.1 kg O2/(m3 d) though fast declining towards a much slower rate. A mass balance of carbon (TOC/TIC) shows that only 10% of the accumulated TOC was transformed to TIC during the 12 hour long experiment. The pilot scale hydrolysis experiment was performed in a new type of biofilm reactor - the B2A® biofilter that is characterised by a series of decreasing sized granular media (80-2.5 mm). When hydrolysis experiments were performed on the anoxic pilot biofilter with pre-screened wastewater particulates as carbon source, a rapid (rV, NO3=0.7 kg NO3-N/(m3 d)) and a slowler (rV, NO3 = 0.3 kg NO3-N/(m3 d)) removal rate were observed at an oxygen concentration of 3.5 mg O2/l. It was found that the pilot biofilter could retain significant amounts of particulate organic matter, reducing the porosity of the filter media of an average from 0.35 to 0.11. A mass balance of carbon shows that up to 40% of the total incoming TOC accumulates in the filter at high flow rates. Only up to 15% of the accumulated TOC was transformed to TIC during the 24 hour long experiment.


2002 ◽  
Vol 45 (6) ◽  
pp. 25-40 ◽  
Author(s):  
E. Morgenroth ◽  
R. Kommedal ◽  
P. Harremoës

Carbon cycling and the availability of organic carbon for nutrient removal processes are in most wastewater treatment systems restricted by the rate of hydrolysis of slowly biodegradable (particulate) organic matter. To date, the mechanisms of hydrolysis are not well understood for complex substrates and mixed populations. Most mathematical models use a simple one-step process to describe hydrolysis. In this article, mechanisms of hydrolysis and mathematical models to describe these processes in wastewater treatment processes are reviewed. Experimental techniques to determine mechanisms of hydrolysis and rate constants are discussed.


Chemosphere ◽  
2021 ◽  
Vol 263 ◽  
pp. 128329 ◽  
Author(s):  
Alondra Alvarado ◽  
Stephanie West ◽  
Gudrun Abbt-Braun ◽  
Harald Horn

Agronomie ◽  
2002 ◽  
Vol 22 (7-8) ◽  
pp. 777-787 ◽  
Author(s):  
Graeme D. Schwenke ◽  
Warwick L. Felton ◽  
David F. Herridge ◽  
Dil F. Khan ◽  
Mark B. Peoples

2020 ◽  
Vol 644 ◽  
pp. 91-103
Author(s):  
D Bearham ◽  
MA Vanderklift ◽  
RA Downie ◽  
DP Thomson ◽  
LA Clementson

Benthic suspension feeders, such as bivalves, potentially have several different food sources, including plankton and resuspended detritus of benthic origin. We hypothesised that suspension feeders are likely to feed on detritus if it is present. This inference would be further strengthened if there was a correlation between δ13C of suspension feeder tissue and δ13C of particulate organic matter (POM). Since detritus is characterised by high particulate organic matter (POC):chl a ratios, we would also predict a positive correlation between POM δ13C and POC:chl a. We hypothesised that increasing depth and greater distance from shore would produce a greater nutritional reliance by experimentally transplanted blue mussels Mytilus edulis on plankton rather than macrophyte-derived detritus. After deployments of 3 mo duration in 2 different years at depths from 3 to 40 m, M. edulis sizes were positively correlated with POM concentrations. POC:chl a ratios and δ13C of POM and M. edulis gill tissue decreased with increasing depth (and greater distance from shore). δ13C of POM was correlated with δ13C of M. edulis. Our results suggest that detritus comprised a large proportion of POM at shallow depths (<15 m), that M. edulis ingested and assimilated carbon in proportion to its availability in POM, and that growth of M. edulis was higher where detritus was present and POM concentrations were higher.


Sign in / Sign up

Export Citation Format

Share Document