Marine planktonic archaea are widespread and abundant in deep oceanic waters but, despite their obvious ecological importance, little is known about them. Metagenomic analyses of large genome fragments allow access to both gene content and genome structure from single individuals of these cultivation-reluctant organisms. We present the comparative analysis of 22 archaeal genomic clones containing 16S rRNA genes that were selected from four metagenomic libraries constructed from meso- and bathypelagic plankton of different oceanic regions (South Atlantic, Antarctic Polar Front, Adriatic and Ionian Sea; depths from 500 to 3000 m). We sequenced clones of the divergent archaeal lineages Group 1A (Crenarchaeota) and Group III (Euryarchaeota) as well as clones from the more frequent Group I Crenarchaeota and Group II Euryarchaeota. Whenever possible, we analysed clones that had identical or nearly identical 16S rRNA genes and that were retrieved from distant geographical locations, that is, that defined pan-oceanic operational taxonomic units (OTUs). We detected genes involved in nitrogen fixation in Group 1A Crenarchaeota, and genes involved in carbon fixation pathways and oligopeptide importers in Group I Crenarchaeota, which could confirm the idea that these are mixotrophic. A two-component system resembling that found in ammonia-oxidizing bacteria was found in Group III Euryarchaeota, while genes for anaerobic respiratory chains were detected in Group II Euryarchaeota. Whereas gene sequence conservation was high, and recombination and gene shuffling extensive within and between OTUs in Group I Crenarchaeota, gene sequence conservation was low and global synteny maintained in Group II Euryarchaeota. This implies remarkable differences in genome dynamics in Group I Crenarchaeota and Group II Euryarchaeota with recombination and mutation being, respectively, the dominant genome-shaping forces. These observations, along with variations in GC content, led us to hypothesize that the two groups of organisms have fundamentally different lifestyles.