TY - JOUR
T1 - Ecophysiological Study of Paraburkholderia sp. Strain 1N under Soil Solution Conditions
T2 - Dynamic Substrate Preferences and Characterization of Carbon Use Efficiency
AU - Cyle, K. Taylor
AU - Klein, Annaleise R.
AU - Aristilde, Ludmilla
AU - Martínez, Carmen Enid
N1 - Funding Information:
Graduate financial support for K.T.C. was provided by the College of Agriculture and Life Sciences at Cornell University. Partial graduate financial support and funding was provided by the Cornell University Program in Cross-Scale Biogeochemistry and Climate, which is supported by NSF-IGERT and the Atkinson Center for a Sustainable Future. Postdoctoral support for A.R.K. was provided by a National Science Foundation CAREER grant (award 1653092) awarded to L.A. This work was also supported by the AFRI Education and Workforce Development Program, grant no. 2019-67011-29513, from the U.S. Department of Agriculture, National Institute of Food and Agriculture.
Funding Information:
Graduate financial support for K.T.C. was provided by the College of Agriculture and Life Sciences at Cornell University. Partial graduate financial support and funding was provided by the Cornell University Program in Cross-Scale Biogeochemistry and Climate, which is supported by NSF-IGERT and the Atkinson Center for a Sustainable Future. Postdoctoral support for A.R.K. was provided by a National Science Foundation CAREER grant (award 1653092) awarded to L.A. This work was also supported by the AFRI Education and Workforce Development Program, grant no. 2019-67011-29513, from the U.S. Department of Agriculture, National Institute of Food and Agriculture. We thank Roland Wilhelm from the Buckley Research Group at Cornell University for his immense help in DNA extraction, genomic sequencing, fruitful discussions on Paraburkholderia, and early edits to the manuscript. We thank the Martínez Research Group members for helpful revisions to the manuscript. Sequencing was performed by the Biotechnology Resource Center (BRC) Genomics Facility at Cornell University (http://www.biotech.cornell.edu/brc/genomics-facility). 1H NMR experiments were performed at the Cornell University NMR facility in the Department of Chemistry and Chemical Biology.
Publisher Copyright:
© 2020. All Rights Reserved.
PY - 2020/12
Y1 - 2020/12
N2 - We used time-resolved metabolic footprinting, an important technical approach used to monitor changes in extracellular compound concentrations during microbial growth, to study the order of substrate utilization (i.e., substrate preferences) and kinetics of a fast-growing soil isolate, Paraburkholderia sp. strain 1N. The growth of Paraburkholderia sp. 1N was monitored under aerobic conditions in a soilextracted solubilized organic matter medium, representing a realistic diversity of available substrates and gradient of initial concentrations. We combined multiple analytical approaches to track over 150 compounds in the medium and complemented this with bulk carbon and nitrogen measurements, allowing estimates of carbon use efficiency throughout the growth curve. Targeted methods allowed the quantification of common low-molecular-weight substrates: glucose, 20 amino acids, and 9 organic acids. All targeted compounds were depleted from the medium, and depletion followed a sigmoidal curve where sufficient data were available. Substrates were utilized in at least three distinct temporal clusters as Paraburkholderia sp. 1N produced biomass at a cumulative carbon use efficiency of 0.43. The two substrates with highest initial concentrations, glucose and valine, exhibited longer usage windows, at higher biomass-normalized rates, and later in the growth curve. Contrary to hypotheses based on previous studies, we found no clear relationship between substrate nominal oxidation state of carbon (NOSC) or maximal growth rate and the order of substrate depletion. Under soil solution conditions, the growth of Paraburkholderia sp. 1N induced multiauxic substrate depletion patterns that could not be explained by the traditional paradigm of catabolite repression.
AB - We used time-resolved metabolic footprinting, an important technical approach used to monitor changes in extracellular compound concentrations during microbial growth, to study the order of substrate utilization (i.e., substrate preferences) and kinetics of a fast-growing soil isolate, Paraburkholderia sp. strain 1N. The growth of Paraburkholderia sp. 1N was monitored under aerobic conditions in a soilextracted solubilized organic matter medium, representing a realistic diversity of available substrates and gradient of initial concentrations. We combined multiple analytical approaches to track over 150 compounds in the medium and complemented this with bulk carbon and nitrogen measurements, allowing estimates of carbon use efficiency throughout the growth curve. Targeted methods allowed the quantification of common low-molecular-weight substrates: glucose, 20 amino acids, and 9 organic acids. All targeted compounds were depleted from the medium, and depletion followed a sigmoidal curve where sufficient data were available. Substrates were utilized in at least three distinct temporal clusters as Paraburkholderia sp. 1N produced biomass at a cumulative carbon use efficiency of 0.43. The two substrates with highest initial concentrations, glucose and valine, exhibited longer usage windows, at higher biomass-normalized rates, and later in the growth curve. Contrary to hypotheses based on previous studies, we found no clear relationship between substrate nominal oxidation state of carbon (NOSC) or maximal growth rate and the order of substrate depletion. Under soil solution conditions, the growth of Paraburkholderia sp. 1N induced multiauxic substrate depletion patterns that could not be explained by the traditional paradigm of catabolite repression.
KW - carbon use efficiency
KW - ecophysiology, Paraburkholderia
KW - nominal oxidation state of carbon
KW - time-resolved metabolic footprinting
UR - http://www.scopus.com/inward/record.url?scp=85096888747&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85096888747&partnerID=8YFLogxK
U2 - 10.1128/AEM.1851-20
DO - 10.1128/AEM.1851-20
M3 - Article
C2 - 33008817
AN - SCOPUS:85096888747
SN - 0099-2240
VL - 86
SP - 1
EP - 18
JO - Applied and Environmental Microbiology
JF - Applied and Environmental Microbiology
IS - 24
ER -