Selective consumption and metabolic allocation of terrestrial and algal carbon determine allochthony in lake bacteria

Aquatic sediments harbour diverse microbial communities that mediate organic matter degradation and influence biogeochemical cycles. The pool of bioavailable carbon continuously changes as a result of abiotic processes and microbial activity. It remains unclear how microbial communities respond to heterogeneous organic matrices and how this ultimately affects heterotrophic respiration. To explore the relationships between the degradation of mixed carbon substrates and microbial activity, we incubated batches of organic-rich sediments in a novel bioreactor (IsoCaRB) that permitted continuous observations of CO production rates, as well as sequential sampling of isotopic signatures (δ C, Δ C), microbial community structure and diversity, and extracellular enzyme activity. Our results indicated that lower molecular weight (MW), labile, phytoplankton-derived compounds were degraded first, followed by petroleum-derived exogenous pollutants, and finally by higher MW polymeric plant material. This shift in utilization coincided with a community succession and increased extracellular enzyme activities. Thus, sequential utilization of different carbon pools induced changes at both the community and cellular level, shifting community composition, enzyme activity, respiration rates, and residual organic matter reactivity. Our results provide novel insight into the accessibility of sedimentary organic matter and demonstrate how bioavailability of natural organic substrates may affect the function and composition of heterotrophic bacterial populations.

Section: Discussionmentioning

confidence: 99%

Sequential bioavailability of sedimentary organic matter to heterotrophic bacteria

Mahmoudi

Beaupré

Steen

et al. 2017

“…Our results do not fully support previous reports on a highly efficient assimilation of OM from various monomers with a generally high total contribution to bacterial biomass production (Kirchman, ), but are rather in agreement with the study of Guillemette et al . () reporting that alga‐derived, carbohydrate‐rich C was preferentially allocated for respiration by lake bacteria. Overall, bacterial OM consumption was directly proportional to the standing stock (i.e., quantity) of different OM compounds released by each alga suggesting non‐selective substrate consumption, as reported for marine bacterioplankton assimilating algal exudates (Sarmento et al ., ).…”

Section: Discussionmentioning

confidence: 99%

Strain‐specific consumption and transformation of alga‐derived dissolved organic matter by members of the Limnohabitans‐C and Polynucleobacter‐B clusters of Betaproteobacteria

Horňák

Kasalický

Šimek

et al. 2017

We investigated changes in quality and quantity of extracellular and biomass-derived organic matter (OM) from three axenic algae (genera Rhodomonas, Chlamydomonas, Coelastrum) during growth of Limnohabitans parvus, Limnohabitans planktonicus and Polynucleobacter acidiphobus representing important clusters of freshwater planktonic Betaproteobacteria. Total extracellular and biomass-derived OM concentrations from each alga were approximately 20 mg l and 1 mg l respectively, from which up to 9% could be identified as free carbohydrates, polyamines, or free and combined amino acids. Carbohydrates represented 54%-61% of identified compounds of the extracellular OM from each alga. In biomass-derived OM of Rhodomonas and Chlamydomonas 71%-77% were amino acids and polyamines, while in that of Coelastrum 85% were carbohydrates. All bacteria grew on alga-derived OM of Coelastrum, whereas only Limnohabitans strains grew on OM from Rhodomonas and Chlamydomonas. Bacteria consumed 24%-76% and 38%-82% of all identified extracellular and biomass-derived OM compounds respectively, and their consumption was proportional to the concentration of each OM compound in the different treatments. The bacterial biomass yield was higher than the total identifiable OM consumption indicating that bacteria also utilized other unidentified alga-derived OM compounds. Bacteria, however, also produced specific OM compounds suggesting enzymatic polymer degradation or de novo exudation.

“…In any case, it is believed that the main role of glycolate in heterotrophic metabolism is as an energy source (Wright and Shah, 1977;Edenborn and Litchfield, 1987). Recently, a study of carbon utilization in temperate lakes showed that a relatively larger portion of phytoplanktonderived carbon was allocated to respiration (and hence energy conservation), while terrestrial carbon was allocated to biosynthesis (Guillemette et al, 2016). Therefore, glycolate may be an important contributor to the maintenance energy of a persisting cell or could facilitate growth by serving as an energy source, fuelling the subsequent assimilation of terrestrial carbon in winter.…”

Section: Verrucomicrobia-phytoplankton Couplingmentioning

confidence: 99%

Microbial life under ice: Metagenome diversity and in situ activity of Verrucomicrobia in seasonally ice‐covered Lakes

Tran

Ramachandran

Khawasik

et al. 2018

Northern lakes are ice-covered for a large part of the year, yet our understanding of microbial diversity and activity during winter lags behind that of the ice-free period. In this study, we investigated under-ice diversity and metabolism of Verrucomicrobia in seasonally ice-covered lakes in temperate and boreal regions of Quebec, Canada using 16S rRNA sequencing, metagenomics and metatranscriptomics. Verrucomicrobia, particularly the V1, V3 and V4 subdivisions, were abundant during ice-covered periods. A diversity of Verrucomicrobia genomes were reconstructed from Quebec lake metagenomes. Several genomes were associated with the ice-covered period and were represented in winter metatranscriptomes, supporting the notion that Verrucomicrobia are metabolically active under ice. Verrucomicrobia transcriptome analysis revealed a range of metabolisms potentially occurring under ice, including carbohydrate degradation, glycolate utilization, scavenging of chlorophyll degradation products, and urea use. Genes for aerobic sulfur and hydrogen oxidation were expressed, suggesting chemolithotrophy may be an adaptation to conditions where labile carbon may be limited. The expression of genes for flagella biosynthesis and chemotaxis was detected, suggesting Verrucomicrobia may be actively sensing and responding to winter nutrient pulses, such as phytoplankton blooms. These results increase our understanding on the diversity and metabolic processes occurring under ice in northern lakes ecosystems.© 2018 Society for Applied Microbiology and John Wiley & Sons Ltd.