Origin of biogeographically distinct ecotypes during laboratory evolution

• Published in: Nature communications Vol. 15; no. 1; pp. 7451 - 14
• Main Authors: Valenzuela, Jacob J., Immanuel, Selva Rupa Christinal, Wilson, James, Turkarslan, Serdar, Ruiz, Maryann, Gibbons, Sean M., Hunt, Kristopher A., Stopnisek, Nejc, Auer, Manfred, Zemla, Marcin, Stahl, David A., Baliga, Nitin S.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 28-08-2024; Nature Publishing Group; Nature Portfolio
• Subjects: 38/23; 38/91; 631/181/2475; 631/326/2565/855; 704/158/857; Affinity; Desulfovibrio vulgaris - genetics; Desulfovibrio vulgaris - metabolism; Directed Molecular Evolution; Ecotype; Ecotypes; Evolution; Fluidized bed reactors; Fluidized beds; Groundwater; Humanities and Social Sciences; Hydrogen - metabolism; Hydrogenase; Methane; Methane - metabolism; Methanococcus - genetics; Methanococcus - metabolism; Microbial activity; Microbiomes; Microbiota - genetics; Microorganisms; multidisciplinary; Mutation; Niches; Partitioning; Productivity; Resource partitioning; Science; Science (multidisciplinary); Subpopulations
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-51759-y

Resource partitioning is central to the incredible productivity of microbial communities, including gigatons in annual methane emissions through syntrophic interactions. Previous work revealed how a sulfate reducer (
Desulfovibrio vulgaris
, Dv) and a methanogen (
Methanococcus maripaludis
, Mm) underwent evolutionary diversification in a planktonic context, improving stability, cooperativity, and productivity within 300–1000 generations. Here, we show that mutations in just 15 Dv and 7 Mm genes within a minimal assemblage of this evolved community gave rise to co-existing ecotypes that were spatially enriched within a few days of culturing in a fluidized bed reactor. The spatially segregated communities partitioned resources in the simulated subsurface environment, with greater lactate utilization by attached Dv but partial utilization of resulting H
2
by low affinity hydrogenases of Mm in the same phase. The unutilized H
2
was scavenged by high affinity hydrogenases of planktonic Mm, producing copious amounts of methane. Our findings show how a few mutations can drive resource partitioning amongst niche-differentiated ecotypes, whose interplay synergistically improves productivity of the entire mutualistic community.
Microbial communities drive all biogeochemical processes on Earth through spatiotemporal resource partitioning. This study shows how a few mutations in an evolved community can result in niche-differentiated ecotypes, whose interplay synergistically improves productivity of the interacting community across sediment and groundwater subpopulations.