Metabolic streamlining in an open-ocean nitrogen-fixing cyanobacterium.
Nitrogen (N(2))-fixing marine cyanobacteria are an important source of fixed inorganic nitrogen that supports oceanic primary productivity and carbon dioxide removal from the atmosphere. A globally distributed, periodically abundant N(2)-fixing marine cyanobacterium, UCYN-A, was recently found to lack the oxygen-producing photosystem II complex of the photosynthetic apparatus, indicating a novel metabolism, but remains uncultivated. Here we show, from metabolic reconstructions inferred from the assembly of the complete UCYN-A genome using massively parallel pyrosequencing of paired-end reads, that UCYN-A has a photofermentative metabolism and is dependent on other organisms for essential compounds. We found that UCYN-A lacks a number of major metabolic pathways including the tricarboxylic acid cycle, but retains sufficient electron transport capacity to generate energy and reducing power from light. Unexpectedly, UCYN-A has a reduced genome (1.44 megabases) that is structurally similar to many chloroplasts and some bacteria, in that it contains inverted repeats of ribosomal RNA operons. The lack of biosynthetic pathways for several amino acids and purines suggests that this organism depends on other organisms, either in close association or in symbiosis, for critical nutrients. However, size fractionation experiments using natural populations have so far not provided evidence of a symbiotic association with another microorganism. The UCYN-A cyanobacterium is a paradox in evolution and adaptation to the marine environment, and is an example of the tight metabolic coupling between microorganisms in oligotrophic oceanic microbial communities.
Tripp
H James
HJ
Ocean Sciences Department, University of California, Santa Cruz, 1156 High Street, Santa Cruz, California 95064, USA.
Bench
Shellie R
SR
Turk
Kendra A
KA
Foster
Rachel A
RA
Desany
Brian A
BA
Niazi
Faheem
F
Affourtit
Jason P
JP
Zehr
Jonathan P
JP
D002244:Carbon / Q000378:metabolism; D002876:Chromosomes, Bacterial / Q000235:genetics; D000458:Cyanobacteria / Q000145:classification / Q000166:cytology / Q000235:genetics* / Q000378:metabolism*; D004579:Electron Transport; D016680:Genome, Bacterial / Q000235:genetics*; D023281:Genomics; D008386:Marine Biology; D008969:Molecular Sequence Data; D009584:Nitrogen / Q000378:metabolism*; D009586:Nitrogen Fixation / Q000235:genetics / Q000502:physiology*; D009792:Oceans and Seas; D010088:Oxidoreductases / Q000235:genetics; D012623:Seawater / Q000382:microbiology*
D002244:Carbon; D010088:Oxidoreductases; C029130:nitrogenase reductase; D009584:Nitrogen