Microbial Domains in the Ocean: A Lesson from the Archaea

NEw ViEws OF sEA MicrOBEs Microbial life thrives in virtually every habitat imaginable in the ocean, from the scalding temperatures found at hydrothermal vents, to frigid environments in and under polar sea ice, to high-pressure habitats in the ocean’s deepest trenches. Our understanding of microbial life in many of these ocean habitats, especially in plankton, has advanced remarkably over the past 30 years or so. The recognition of the ubiquity and distribution of photoautotrophic cyanobacteria such as Synechococcus and Prochlorococcus (Johnson and Sieburth, 1979; Waterbury et al., 1979; Chisholm et al., 1988), the isolation of pressure-requiring piezophilic bacteria (Yayanos et al., 1979), the discovery of Pelagibacter (Giovannoni et al., 1990), and recognition of the high abundance of marine phage (Bergh et al., 1989) represent just a few recent milestones in microbial oceanography. Even at a level as fundamental as the distribution of life’s three major domains (Bacteria, Archaea, and Eukarya), it is only recently that a clear picture of “who lives where” in the ocean has emerged. From the standpoint of oceanography, why should we care about microbial

tion of the ubiquity and distribution of photoautotrophic cyanobacteria such as Synechococcus and Prochlorococcus (Johnson and Sieburth, 1979;Waterbury et al., 1979;Chisholm et al., 1988), the isolation of pressure-requiring piezophilic bacteria (Yayanos et al., 1979), the discovery of Pelagibacter (Giovannoni et al., 1990), and recognition of the high abundance of marine phage (Bergh et al., 1989) represent just a few recent milestones in microbial oceanography. Pace and Stephen Giovannoni, and later others, in the early 1990s, proved to be reasonably productive enterprises. A strong motivation for these microbial surveys was the general recognition that microbial activities drive most of the major biogeochemical cycles in the sea.
Furthermore, it was suspected that many dominant planktonic microbial groups might be undetected because of their recalcitrance to cultivation. Given the "great plate count anomaly" (e.g., the observation that cultivable planktonic microbes accounted for only a small percentage of total direct epifluorescence microscopic counts [Staley and Konopka, 1985] This article has been published in Oceanography, Volume 20, Number 2, a quarterly journal of The Oceanography society. copyright 2007 by The Oceanography society. All rights reserved. permission is granted to copy this article for use in teaching and research. republication, systemmatic reproduction, or collective redistirbution of any portion of this article by photocopy machine, reposting, or other means is permitted only with the approval of The Oceanography society. send all correspondence to: info@tos.org or Th e Oceanography society, pO Box 1931, rockville, MD 20849-1931 biogeochemical cycling processes, likely remained unknown. This presumption turned out to be more or less correct. A fundamental advance that accelerated relatively unbiased microbial census taking was the invention by Norm Pace and collaborators of cultivationindependent, molecular-phylogenetic survey approaches (Olsen et al., 1986).
This strategy uses common molecular sequences found in every cell (e.g., ribosomal RNA sequence) that can serve as a sort barcode to identify and track microbes by "reading" DNA sequences extracted directly from the environment, without the need for cultivation.

O cE ANic ArchAE A?
The Archaea are a curious phylogenetic domain (formerly kingdom) comprised of an odd assortment of cultured microbes that fall into three major groupings: extreme halophiles, methanogens, and extreme thermophiles and thermoacidophiles (Woese, 1987). Why such an odd assortment of salt-loving, or anaerobic, or heat-loving microbes should form such a coherent phylogenetic grouping is still not that well understood. The dogma until 1992 was that archaea inhabit mainly ...it is only recently that a clear picture of "who lives where" in the ocean has emerged.
Following on the heels of these first oceanic sightings, archaeal groups began cropping up in many unexpected habitats. The next steps were to quantify the distribution and abundance of these unusual microbes and to begin to understand their biological properties and ecological significance.

DistriButiON, AND VAriABiLity
Once it was clear that archaea were reasonably abundant players in microbial plankton, scientists initiated studies that employed radiolabeled, archaeaspecific oligonucleotide probes to quantify total, extractable archaeal rRNA in marine plankton (Figure 1). Surprisingly, planktonic Crenarchaea were found to contribute as much as 20% to the total microbial rRNA in late-winter Antarctic coastal waters at -1. 8°C (DeLong et al., 1994). Surveys in temperate waters off the coast of California also showed that the planktonic Crenarchaea tended to be most abundant in waters below the euphotic zone (Massana et al., 1997). This trend has generally held  (DeLong et al., 1998). In addition, Preston et al. (1996) showed that Cenarchaeum symbiosum, a crenarchaeal    (Treusch et al., 2005). This new archaeal ammonia monooxygenase gene was subsequently detected in many marine environments as well (Wuchter et al., 2006;Mincer et al., 2007). Genomic analyses subsequently revealed many other genes associated with nitrification and CO 2 fixation in marine Crenarchaea (Hallam et al., 2006a(Hallam et al., , 2006b (Francis et al., 2007).
New observations on the biology, ecology, and activity of planktonic Crenarchaea continue to accumulate.
These include detailed quantitative analyses modeling in situ carbon sources of planktonic Crenarchaea (Ingalls et al., 2006), microautoradiography studies to track substrate assimilation into different cell types (Herndl et al., 2005), and observations of Crenarchaea in anoxic zones of the Black Sea (Coolen et al., 2007) and the Arabian Sea (Damste et al., 2002).