Open AccessPatterns of ecological specialization among microbial populations in the R ed S ea and diverse oligotrophic marine environments
Author(s) -
Thompson Luke R.,
Field Chris,
Romanuk Tamara,
Ngugi David,
Siam Rania,
Dorry Hamza,
Stingl Ulrich
Publication year - 2013
Publication title -
ecology and evolution
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.17
H-Index - 63
ISSN - 2045-7758
DOI - 10.1002/ece3.593
Subject(s) - ecotype , biology , metagenomics , salinity , cyanobacteria , adaptation (eye) , osmolyte , microbial mat , synechococcus , prochlorococcus , photoprotection , extreme environment , ecology , extremophile , pelagic zone , gene , botany , photosynthesis , bacteria , genetics , neuroscience , thermophile
Large swaths of the nutrient‐poor surface ocean are dominated numerically by cyanobacteria ( P rochlorococcus ), cyanobacterial viruses (cyanophage), and alphaproteobacteria ( SAR 11). How these groups thrive in the diverse physicochemical environments of different oceanic regions remains poorly understood. Comparative metagenomics can reveal adaptive responses linked to ecosystem‐specific selective pressures. The R ed S ea is well‐suited for studying adaptation of pelagic‐microbes, with salinities, temperatures, and light levels at the extreme end for the surface ocean, and low nutrient concentrations, yet no metagenomic studies have been done there. The R ed S ea (high salinity, high light, low N and P) compares favorably with the M editerranean S ea (high salinity, low P), S argasso S ea (low P), and N orth P acific S ubtropical G yre (high light, low N). We quantified the relative abundance of genetic functions among P rochlorococcus , cyanophage, and SAR 11 from these four regions. Gene frequencies indicate selection for phosphorus acquisition ( M editerranean/ S argasso), DNA repair and high‐light responses ( R ed S ea/ P acific P rochlorococcus ), and osmolyte C1 oxidation ( R ed S ea/ M editerranean SAR 11). The unexpected connection between salinity‐dependent osmolyte production and SAR 11 C1 metabolism represents a potentially major coevolutionary adaptation and biogeochemical flux. Among P rochlorococcus and cyanophage, genes enriched in specific environments had ecotype distributions similar to nonenriched genes, suggesting that inter‐ecotype gene transfer is not a major source of environment‐specific adaptation. Clustering of metagenomes using gene frequencies shows similarities in populations ( R ed S ea with P acific, M editerranean with S argasso) that belie their geographic distances. Taken together, the genetic functions enriched in specific environments indicate competitive strategies for maintaining carrying capacity in the face of physical stressors and low nutrient availability.