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Ecological distribution and population physiology defined by proteomics in a natural microbial community.

Mueller RS, Denef VJ, Kalnejais LH, Suttle KB, Thomas BC, Wilmes P, Smith RL, Nordstrom DK, McCleskey RB, Shah MB, Verberkmoes NC, Hettich RL, Banfield JF - Mol. Syst. Biol. (2010)

Bottom Line: Its overall physiology is robust to abiotic environmental factors, but strong correlations exist between these factors and certain subsets of proteins, possibly accounting for its wide environmental distribution.Lower abundance populations are patchier in their distribution, and proteomic data indicate that their environmental niches may be constrained by specific sets of abiotic environmental factors.This research establishes an effective strategy to investigate ecological relationships between microbial physiology and the environment for whole communities in situ.

View Article: PubMed Central - PubMed

Affiliation: Earth and Planetary Science Department, University of California, Berkeley, CA 94720, USA.

ABSTRACT
An important challenge in microbial ecology is developing methods that simultaneously examine the physiology of organisms at the molecular level and their ecosystem level interactions in complex natural systems. We integrated extensive proteomic, geochemical, and biological information from 28 microbial communities collected from an acid mine drainage environment and representing a range of biofilm development stages and geochemical conditions to evaluate how the physiologies of the dominant and less abundant organisms change along environmental gradients. The initial colonist dominates across all environments, but its proteome changes between two stable states as communities diversify, implying that interspecies interactions affect this organism's metabolism. Its overall physiology is robust to abiotic environmental factors, but strong correlations exist between these factors and certain subsets of proteins, possibly accounting for its wide environmental distribution. Lower abundance populations are patchier in their distribution, and proteomic data indicate that their environmental niches may be constrained by specific sets of abiotic environmental factors. This research establishes an effective strategy to investigate ecological relationships between microbial physiology and the environment for whole communities in situ.

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Correlations of proteins of Leptospirillum Group II with environmental factors. (A) Clustering of samples using abundance values of differentially detected proteins (significance analysis of microarrays with a false-discovery rate <0.05) of Leptospirillum Group II (474 proteins, see Supplementary Table S4 for the complete list of proteins). Column labels signify sample names and green and blue highlights represent expression group designation from Figure 2. (B) Functional differences of Leptospirillum Group II between developmental stages. Values represent the bias in total proteins overrepresented in either high or low developmental stages. Positive values (blue bars) signify categories overrepresented in high developmental stage biofilms and negative values (green bars) signify categories overrepresented in low developmental stage biofilms. Asterisks note categories significantly overrepresented (98% confidence interval). (C) Pairwise scatter plots of measurements of selected environmental factors strongly correlated to the abundances of a given protein. Source data is available for this figure at www.nature.com/msb.
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f4: Correlations of proteins of Leptospirillum Group II with environmental factors. (A) Clustering of samples using abundance values of differentially detected proteins (significance analysis of microarrays with a false-discovery rate <0.05) of Leptospirillum Group II (474 proteins, see Supplementary Table S4 for the complete list of proteins). Column labels signify sample names and green and blue highlights represent expression group designation from Figure 2. (B) Functional differences of Leptospirillum Group II between developmental stages. Values represent the bias in total proteins overrepresented in either high or low developmental stages. Positive values (blue bars) signify categories overrepresented in high developmental stage biofilms and negative values (green bars) signify categories overrepresented in low developmental stage biofilms. Asterisks note categories significantly overrepresented (98% confidence interval). (C) Pairwise scatter plots of measurements of selected environmental factors strongly correlated to the abundances of a given protein. Source data is available for this figure at www.nature.com/msb.

Mentions: Of the 474 Leptospirillum Group II proteins that showed a significant relationship with CS, 370 are overrepresented in high and 104 in low developmental stage biofilms. Clustering of samples using these proteins revealed two metabolic states when growing within low versus high developmental stage biofilms with high within-cluster correlations (r̄=0.89±0.05; Pearson correlation coefficient; Figure 4A). Leptospirillum Group II proteins associated with this metabolic reorganization were grouped into functional categories and significant biases were defined. Ribosome biosynthesis, which includes ribosome structural proteins, and transcription, which includes RNA polymerase proteins and proteins involved in transcriptional regulation, were significantly elevated in low developmental stage biofilms, as well as proteins involved in physical and chemical stress defense, unknown functions, and associated with mobile genetic elements (Figure 4B). In the high developmental stage biofilms, we detected increased investment in proteins involved in chaperone and protein turnover functions, and environmental signaling, chemotaxis, and motility (Figure 4B). There was also a shift in metabolism away from ribosome biosynthesis towards proteins involved in biosynthesis of extracellular components, carbohydrates, and amino acids.


Ecological distribution and population physiology defined by proteomics in a natural microbial community.

Mueller RS, Denef VJ, Kalnejais LH, Suttle KB, Thomas BC, Wilmes P, Smith RL, Nordstrom DK, McCleskey RB, Shah MB, Verberkmoes NC, Hettich RL, Banfield JF - Mol. Syst. Biol. (2010)

Correlations of proteins of Leptospirillum Group II with environmental factors. (A) Clustering of samples using abundance values of differentially detected proteins (significance analysis of microarrays with a false-discovery rate <0.05) of Leptospirillum Group II (474 proteins, see Supplementary Table S4 for the complete list of proteins). Column labels signify sample names and green and blue highlights represent expression group designation from Figure 2. (B) Functional differences of Leptospirillum Group II between developmental stages. Values represent the bias in total proteins overrepresented in either high or low developmental stages. Positive values (blue bars) signify categories overrepresented in high developmental stage biofilms and negative values (green bars) signify categories overrepresented in low developmental stage biofilms. Asterisks note categories significantly overrepresented (98% confidence interval). (C) Pairwise scatter plots of measurements of selected environmental factors strongly correlated to the abundances of a given protein. Source data is available for this figure at www.nature.com/msb.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2913395&req=5

f4: Correlations of proteins of Leptospirillum Group II with environmental factors. (A) Clustering of samples using abundance values of differentially detected proteins (significance analysis of microarrays with a false-discovery rate <0.05) of Leptospirillum Group II (474 proteins, see Supplementary Table S4 for the complete list of proteins). Column labels signify sample names and green and blue highlights represent expression group designation from Figure 2. (B) Functional differences of Leptospirillum Group II between developmental stages. Values represent the bias in total proteins overrepresented in either high or low developmental stages. Positive values (blue bars) signify categories overrepresented in high developmental stage biofilms and negative values (green bars) signify categories overrepresented in low developmental stage biofilms. Asterisks note categories significantly overrepresented (98% confidence interval). (C) Pairwise scatter plots of measurements of selected environmental factors strongly correlated to the abundances of a given protein. Source data is available for this figure at www.nature.com/msb.
Mentions: Of the 474 Leptospirillum Group II proteins that showed a significant relationship with CS, 370 are overrepresented in high and 104 in low developmental stage biofilms. Clustering of samples using these proteins revealed two metabolic states when growing within low versus high developmental stage biofilms with high within-cluster correlations (r̄=0.89±0.05; Pearson correlation coefficient; Figure 4A). Leptospirillum Group II proteins associated with this metabolic reorganization were grouped into functional categories and significant biases were defined. Ribosome biosynthesis, which includes ribosome structural proteins, and transcription, which includes RNA polymerase proteins and proteins involved in transcriptional regulation, were significantly elevated in low developmental stage biofilms, as well as proteins involved in physical and chemical stress defense, unknown functions, and associated with mobile genetic elements (Figure 4B). In the high developmental stage biofilms, we detected increased investment in proteins involved in chaperone and protein turnover functions, and environmental signaling, chemotaxis, and motility (Figure 4B). There was also a shift in metabolism away from ribosome biosynthesis towards proteins involved in biosynthesis of extracellular components, carbohydrates, and amino acids.

Bottom Line: Its overall physiology is robust to abiotic environmental factors, but strong correlations exist between these factors and certain subsets of proteins, possibly accounting for its wide environmental distribution.Lower abundance populations are patchier in their distribution, and proteomic data indicate that their environmental niches may be constrained by specific sets of abiotic environmental factors.This research establishes an effective strategy to investigate ecological relationships between microbial physiology and the environment for whole communities in situ.

View Article: PubMed Central - PubMed

Affiliation: Earth and Planetary Science Department, University of California, Berkeley, CA 94720, USA.

ABSTRACT
An important challenge in microbial ecology is developing methods that simultaneously examine the physiology of organisms at the molecular level and their ecosystem level interactions in complex natural systems. We integrated extensive proteomic, geochemical, and biological information from 28 microbial communities collected from an acid mine drainage environment and representing a range of biofilm development stages and geochemical conditions to evaluate how the physiologies of the dominant and less abundant organisms change along environmental gradients. The initial colonist dominates across all environments, but its proteome changes between two stable states as communities diversify, implying that interspecies interactions affect this organism's metabolism. Its overall physiology is robust to abiotic environmental factors, but strong correlations exist between these factors and certain subsets of proteins, possibly accounting for its wide environmental distribution. Lower abundance populations are patchier in their distribution, and proteomic data indicate that their environmental niches may be constrained by specific sets of abiotic environmental factors. This research establishes an effective strategy to investigate ecological relationships between microbial physiology and the environment for whole communities in situ.

Show MeSH
Related in: MedlinePlus