Remarkable heterogeneity in meso- and bathypelagic bacterioplankton assemblage composition

We investigated mesoto bathypelagic (500–3,000 m) bacterioplankton assemblage composition at 19 locations in the North Atlantic Ocean beneath the offshore Amazon River plume, in the North Pacific Ocean near the Hawaiian archipelago, at the San Pedro Ocean Time Series (SPOTS) station off southern California, and in the Coral Sea off eastern Australia with a sensitive high-throughput fingerprinting approach, automated rRNA intergenic spacer analysis (ARISA), to examine variation between bacterial assemblages at different stations. Temperature and salinity were used to identify distinct water masses within gyres. ARISA fingerprints each contained 15–117 operational taxonomic units (OTUs) per assemblage; however, the OTU composition of fingerprints varied among stations, even within the same water mass. Fingerprints from 500 m at the SPOTS station over 4 yr shared on average a Sorensen Index (presence/absence similarity) of 0.68 6 0.01 and a Whittaker Index (proportional representation similarity) of 0.68 6 0.01, whereas at more oceanic stations at 500 m, fingerprints shared a Sorensen Index of 0.48 6 0.01 and a Whittaker Index of 0.38 6 0.01. At deeper depths (1,000 and 2,000 m), fingerprints were equally variable, sharing Sorensen Indices of 0.42 6 0.02 and 0.50 6 0.02 and Whittaker indices of 0.33 6 0.01 and 0.34 6 0.03, at 1,000 m and 3,000 m, respectively. Mesopelagic, moderately productive waters were more stable than those at less productive, open-ocean gyre stations, suggesting that variability in bacterioplankton communities at depth is influenced by organic matter supply and patchiness. Bacterioplankton in the world’s oceans are ecologically critical, processing typically 50% of primary production (Fuhrman and Azam 1982; Azam et al. 1983), comprising up to 70% of biomass in surface waters (Fuhrman et al. 1989), and mediating many global-scale nutrient transformations. Despite this, the richness and diversity of planktonic prokaryotic assemblages in the oceans have only recently been studied because of the advent of molecular techniques (Giovannoni et al. 1990; Fuhrman et al. 1992, 1993), which circumvent classical culture biases associated with .99% of bacterial taxa. These studies, and recent advances in molecular approaches to addressing assemblage composition, have revealed an astonishingly high diversity of marine bacterioplankton (Curtis et al. 2002; Venter et al. 2004); however, the distribution of assemblages across a number of environments has not been previously studied, partially because of the extraordinary costs of large-scale sequencing projects. The development of less costly, high-sensitivity and -throughput fingerprinting approaches (Muyzer et al. 1993; Avaniss-Aghajani et al. 1994; Fisher and Triplett 1999) now allows researchers to examine the distribution of entire assemblages across a wider range of samples. Most studies of bacterioplankton assemblages to date have focused upon a handful of samples (Giovannoni et al. 1990; Delong 1992; Fuhrman et al. 1992) or one or two depth intervals (Venter et al. 2004); consequently, spatial variability across habitats has not been investigated extensively. Studies of bacterioplankton diversity via 16S rDNA clone libraries were among the first to reveal novel archaebacterial lineages (Delong 1992; Fuhrman et al. 1992), and demonstrated the predominance of the Chloroflexi-like SAR-202 cluster at depth (Morris et al. 2004). Despite these previous studies, there is almost no information on the spatial variability of meso(500 m) or bathypelagic (1,000–3,000 m) bacterioplankton assemblages. The composition of bacterioplankton communities in the ocean is believed to be influenced by resource availability (Torsvik et al. 2002) and selective loss factors (e.g., bacterivory and viral lysis [Fuhrman 1992; Thingstad and Lignell 1997]). Microbial growth and decay are very slow under cold and high-pressure deep-sea conditions (Jannasch et al. 1970; Cho and Azam 1988; Ducklow and Carlson 1992). This has been dramatically demonstrated by strong preservation of food materials after the accidental sinkings of the HMS Titanic (Holden 1985) and the deep1 To whom correspondence should be addressed. Present address: Department of Ocean Sciences, University of California Santa Cruz, 1156 High Street EMS D446, Santa Cruz, California 95064 ([email protected]). Acknowledgments We thank M. Schwalbach, M. Brown, X. Hernandez, R. Beinart, X. Liang, P.J. Morris, R. Schimmoeler, G. Smith, M. Prokopenko, O. Johnson, and the crews of the research vessels R/ V Sea Watch, R/V Yellowfin, R/V Point Sur, R/V Seward Johnson, R/V Ka‘Imikai-o-Kanaloa, R/V Kilo Moana, and R/V Roger Revelle for assistance with field work. Helpful information was supplied by O. Beja and E. DeLong on unlinked ssu and lsu. We thank the SeaWiFS Project and the Goddard Earth Sciences Data and Information Services Center/Distributed Active Archive Center at the Goddard Space Flight Center, for the production and distribution of the SeaWIFS image, respectively (sponsored by NASA’s Earth Science Enterprise). This work was supported by NSF Grant 0527034 awarded to JAF, DGC, and V. Coles, NSF Microbial Observatories Grant MCB0084231 awarded to JAF and D. Caron, and Biocomplexity grants OCE9981545 awarded to DGC, A. Michaels, and A. Subrumaniam, and OCE9981373 awarded to DGC. This research is in partial fulfilment of a Ph.D. by IH. Limnol. Oceanogr., 51(3), 2006, 1274–1283 E 2006, by the American Society of Limnology and Oceanography, Inc.