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Title: Environmental matrix and moisture are key determinants of microbial phenotypes expressed in a reduced complexity soil-analog

Abstract

Soil moisture and porosity regulate microbial metabolism by influencing factors such as redox conditions, substrate availability, and soil connectivity. However, the inherent biological, chemical, and physical heterogeneity of soil complicates laboratory investigations into microbial phenotypes that mediate community metabolism. This difficulty arises from challenges in accurately representing the soil environment and in establishing a tractable microbial community that limits confounding variables. To address these challenges in our investigation of community metabolism, we use a reduced-complexity microbial consortium grown in a soil analog using a glass-bead matrix amended with chitin. Long-read and short-read metagenomes, metatranscriptomes, metaproteomes, and metabolomes were analyzed to test the effects of soil structure and moisture on chitin degradation. Our soil structure analog system greatly altered microbial expression profiles compared to the liquid-only incubations, emphasizing the importance of incorporating environmental parameters, like pores and surfaces, for understanding microbial phenotypes relevant to soil ecosystems. These changes were mainly driven by differences in overall expression of chitin-degrading Streptomyces species and stress-tolerant Ensifer. Our findings suggest that the success of Ensifer in a structured environment is likely related to its ability to repurpose carbon via the glyoxylate shunt while potentially using polyhydroxyalkanoate granules as a C source. We also identified traitsmore » like motility, stress resistance, and biofilm formation that underlie the degradation of chitin across our treatments and inform how they may ultimately alter carbon use efficiency. Together our results demonstrate that community functions like decomposition are sensitive to environmental conditions and more complex than the multi-enzyme pathways involved in depolymerization.« less

Authors:
; ; ; ; ; ;
  1. Pacific Northwest National Laboratory (PNNL), Richland, WA (United States); Pacific Northwest National Laboratory
  2. Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
  3. Washington State Univ., Pullman, WA (United States)
Publication Date:
Other Number(s):
PNNL-SA-205872
DOE Contract Number:  
AC05-76RL01830
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
2476507
DOI:
https://doi.org/10.25584/2476507

Citation Formats

Rodriguez-Ramos, Josue A, Sadler, Natalie C, Zegeye, Elias, Farris, Yuliya, Purvine, Samuel O, Couvillion, Sneha P, and Hofmockel, Kirsten S. Environmental matrix and moisture are key determinants of microbial phenotypes expressed in a reduced complexity soil-analog. United States: N. p., 2023. Web. doi:10.25584/2476507.
Rodriguez-Ramos, Josue A, Sadler, Natalie C, Zegeye, Elias, Farris, Yuliya, Purvine, Samuel O, Couvillion, Sneha P, & Hofmockel, Kirsten S. Environmental matrix and moisture are key determinants of microbial phenotypes expressed in a reduced complexity soil-analog. United States. doi:https://doi.org/10.25584/2476507
Rodriguez-Ramos, Josue A, Sadler, Natalie C, Zegeye, Elias, Farris, Yuliya, Purvine, Samuel O, Couvillion, Sneha P, and Hofmockel, Kirsten S. 2023. "Environmental matrix and moisture are key determinants of microbial phenotypes expressed in a reduced complexity soil-analog". United States. doi:https://doi.org/10.25584/2476507. https://www.osti.gov/servlets/purl/2476507. Pub date:Sun Dec 31 23:00:00 EST 2023
@article{osti_2476507,
title = {Environmental matrix and moisture are key determinants of microbial phenotypes expressed in a reduced complexity soil-analog},
author = {Rodriguez-Ramos, Josue A and Sadler, Natalie C and Zegeye, Elias and Farris, Yuliya and Purvine, Samuel O and Couvillion, Sneha P and Hofmockel, Kirsten S},
abstractNote = {Soil moisture and porosity regulate microbial metabolism by influencing factors such as redox conditions, substrate availability, and soil connectivity. However, the inherent biological, chemical, and physical heterogeneity of soil complicates laboratory investigations into microbial phenotypes that mediate community metabolism. This difficulty arises from challenges in accurately representing the soil environment and in establishing a tractable microbial community that limits confounding variables. To address these challenges in our investigation of community metabolism, we use a reduced-complexity microbial consortium grown in a soil analog using a glass-bead matrix amended with chitin. Long-read and short-read metagenomes, metatranscriptomes, metaproteomes, and metabolomes were analyzed to test the effects of soil structure and moisture on chitin degradation. Our soil structure analog system greatly altered microbial expression profiles compared to the liquid-only incubations, emphasizing the importance of incorporating environmental parameters, like pores and surfaces, for understanding microbial phenotypes relevant to soil ecosystems. These changes were mainly driven by differences in overall expression of chitin-degrading Streptomyces species and stress-tolerant Ensifer. Our findings suggest that the success of Ensifer in a structured environment is likely related to its ability to repurpose carbon via the glyoxylate shunt while potentially using polyhydroxyalkanoate granules as a C source. We also identified traits like motility, stress resistance, and biofilm formation that underlie the degradation of chitin across our treatments and inform how they may ultimately alter carbon use efficiency. Together our results demonstrate that community functions like decomposition are sensitive to environmental conditions and more complex than the multi-enzyme pathways involved in depolymerization.},
doi = {10.25584/2476507},
journal = {},
number = ,
volume = ,
place = {United States},
year = {Sun Dec 31 23:00:00 EST 2023},
month = {Sun Dec 31 23:00:00 EST 2023}
}