Molecular analysis of picocyanobacterial community structure along an Arabian Sea transect reveals distinct spatial separation of lineages

We investigated the community structure of Synechococcus and Prochlorococcus along a transect in the Arabian Sea during September 2001. The transect spanned contrasting oceanic conditions, allowing investigation of the effects of both horizontal and vertical environmental gradients over relatively large spatial scales on picocyanobacterial population structure. We applied previously developed oligonucleotide probes specific for different Prochlorococcus ecotypes and Synechococcus clades by hybridization to ‘oxygenic phototroph’ 16S ribosomal DNA polymerase chain reaction amplicons. Flow cytometry data showed that, in general, the picocyanobacterial community was dominated by Prochlorococcus in the southern oligotrophic waters and by Synechococcus in the northern mesotrophic waters. Molecular analysis of these picophytoplankton communities, however, revealed more specific spatial separation of lineages along the transect, with Prochlorococcus in southern surface waters being dominated by the high light–adapted ecotype, while low light–adapted (LL) ecotypes were confined to deeper waters below the surface-mixed layer. Interestingly, between Sta. 2 to 4, the LL genotype MIT9303 appeared to be partitioned at the very base of the euphotic zone, beneath other LL genotypes. Most of the central and northern parts of the transect were dominated by Synechococcus genotypes of the clade II lineage. A significant exception was in the mesotrophic upwelling region, where genotypes representative of clades V/VI/ VII dominated. Members of the recently discovered clades IX and X were found in subsurface samples in warm, coastal waters. We propose that discrete differences, both horizontally and vertically, in a suite of environmental parameters along the transect provide optimal growth conditions for specific genotypes in a particular patch of water, giving rise to distinct spatial compartmentalization of picocyanobacterial lineages. Picocyanobacteria of the genera Prochlorococcus and Synechococcus dominate the prokaryotic component of the picophytoplankton of open-ocean environments, contributing over 50% of primary production in some areas (e.g., see Li 1994; Veldhuis et al. 1997; Brown et al. 1999). Work using both cultured isolates and natural populations has shown the two genera to be genetically (Toledo et al. 1999; Rocap et al. 2002; Fuller et al. 2003) and physiologically (see Moore et al. 1995; Palenik 2001; Scanlan 2003) diverse, comprising a number of closely related genotypes or ecotypes. Indeed, it appears that this genetic diversity underlies their ecological success. Thus, for Prochlorococcus, phylogenetically distinct high light (HL)–and low light (LL)–adapted ecotypes exist, these being defined by specific photosynthetic pigment characteristics, photophysiology, and nutrient acquisition profiles (Moore and Chisholm 1999; Moore et al. 2002; Bailey et al. 2005). These HL and LL ecotypes exhibit specific depth-dependent distributions (West and Scanlan 1999; West et al. 2001; Steglich et al. 2003) with the idea that at least vertically down a stratified water column, partitioning of genotypes allows for competitive growth over a broader range of conditions than could be achieved by a genetically homogeneous population. Even for marine Synechococcus, for which the relationship between diversity and physiology is not yet well defined, but in which at least 10 genetic lineages have been defined (Fuller et al. 2003), there is evidence for the specific partitioning of strains, as indicated by the presence of a serotype found preferentially in surface waters (Toledo and Palenik 2003). Evidence thus far indicates, then, that the environmental gradients of light, nutrients, and 1 Present address: Darling Marine Center, University of Maine, Walpole, Maine 04573. 2 Corresponding author ([email protected]). Acknowledgments We thank Jeff Benson for CTD data and Principal Scientist Peter Burkill, Captain Keith Avery, and the crew of the RRS Charles Darwin for excellent logistical support on the AMBITION cruise. This work was supported by NERC grants NER/T/S/2000/ 00621 and GST/02/2819, the former as part of the Marine and Freshwater Microbial Biodiversity program. Support from the Plymouth Marine Laboratory core science program is also acknowledged. Limnol. Oceanogr., 51(6), 2006, 2515–2526 E 2006, by the American Society of Limnology and Oceanography, Inc.