Enhanced nutrient uptake is sufficient to drive emergent cross-feeding between bacteria in a synthetic community
- 12 August 2020
- journal article
- research article
- Published by Oxford University Press (OUP) in The ISME Journal
- Vol. 14 (11), 2816-2828
- https://doi.org/10.1038/s41396-020-00737-5
Abstract
Interactive microbial communities are ubiquitous, influencing biogeochemical cycles and host health. One widespread interaction is nutrient exchange, or cross-feeding, wherein metabolites are transferred between microbes. Some cross-fed metabolites, such as vitamins, amino acids, and ammonium (NH4+), are communally valuable and impose a cost on the producer. The mechanisms that enforce cross-feeding of communally valuable metabolites are not fully understood. Previously we engineered a cross-feeding coculture between N2-fixing Rhodopseudomonas palustris and fermentative Escherichia coli. Engineered R. palustris excretes essential nitrogen as NH4+ to E. coli, while E. coli excretes essential carbon as fermentation products to R. palustris. Here, we sought to determine whether a reciprocal cross-feeding relationship would evolve spontaneously in cocultures with wild-type R. palustris, which is not known to excrete NH4+. Indeed, we observed the emergence of NH4+ cross-feeding, but driven by adaptation of E. coli alone. A missense mutation in E. coli NtrC, a regulator of nitrogen scavenging, resulted in constitutive activation of an NH4+ transporter. This activity likely allowed E. coli to subsist on the small amount of leaked NH4+ and better reciprocate through elevated excretion of fermentation products from a larger E. coli population. Our results indicate that enhanced nutrient uptake by recipients, rather than increased excretion by producers, is an underappreciated yet possibly prevalent mechanism by which cross-feeding can emerge.Keywords
Funding Information
- United States Department of Defense | United States Army | U.S. Army Research, Development and Engineering Command | Army Research Office (W911NF-17-1-0159, W911NF-14-1-0411)
- NSF | BIO | Division of Molecular and Cellular Biosciences (MCB-1749489)
- DOE | SC | Biological and Environmental Research (DE-SC0008131)
- DOE | Office of Science (DE-AC02-05CH11231)
- United States Department of Defense | United States Army | U.S. Army Research, Development and Engineering Command | Army Research Office (W911NF-17-1-0159, W911NF-14-1-0411, W911NF-17-1-0159)
- NSF | BIO | Division of Molecular and Cellular Biosciences (MCB-1749489)
- DOE | SC | Biological and Environmental Research (DE-SC0008131)
- DOE | Office of Science (DE-AC02-05CH11231, DE-AC02-05CH11231)
This publication has 60 references indexed in Scilit:
- From Metabolism to Ecology: Cross-Feeding Interactions Shape the Balance between Polymicrobial Conflict and MutualismThe American Naturalist, 2012
- Adaptation to a new environment allows cooperators to purge cheaters stochasticallyProceedings of the National Academy of Sciences of the United States of America, 2012
- Need‐based activation of ammonium uptake in Escherichia coliMolecular Systems Biology, 2012
- Using artificial systems to explore the ecology and evolution of symbiosesCellular and Molecular Life Sciences, 2011
- Production of Hydrogen Gas from Light and the Inorganic Electron Donor Thiosulfate by Rhodopseudomonas palustrisApplied and Environmental Microbiology, 2010
- Carbon dioxide fixation as a central redox cofactor recycling mechanism in bacteriaProceedings of the National Academy of Sciences of the United States of America, 2010
- Rapid evolution of stability and productivity at the origin of a microbial mutualismProceedings of the National Academy of Sciences of the United States of America, 2010
- Fast and accurate short read alignment with Burrows–Wheeler transformBioinformatics, 2009
- Insights into Actinobacillus succinogenes Fermentative Metabolism in a Chemically Defined Growth MediumApplied and Environmental Microbiology, 2005
- The Complete Genome Sequence of Escherichia coli K-12Science, 1997