Bacterial Community Shifts in Taxa and Diversity in Response to Localized Organic Loading in the Deep Seaemi 2072 344..363
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Environmental Microbiology (2010) 12(2), 344–363 doi:10.1111/j.1462-2920.2009.02072.x Bacterial community shifts in taxa and diversity in response to localized organic loading in the deep seaemi_2072 344..363 Shana K. Goffredi† and Victoria J. Orphan* microbial community to large pulses of organic California Institute of Technology, Pasadena, CA, USA. carbon is complex, likely affected by increased animal bioturbation, and may be sustained over time periods that span years to perhaps even decades. Summary The deep sea is a unique and extreme environment Introduction characterized by low concentrations of highly recal- citrant carbon. As a consequence, large organic Organic material in the oceans, originating from primary inputs have potential to cause significant perturba- production in surface waters, is recycled within the water tion. To assess the impact of organic enrichment on column, leaving only small amounts to aggregate, sink deep sea microbial communities, we investigated and eventually become buried. This sedimentation of bacterial diversity in sediments underlying two whale particulate organic matter to the seafloor results in low falls at 1820 and 2893 m depth in Monterey Canyon, concentrations (< 0.1% by weight) of highly recalcitrant as compared with surrounding reference sediment carbon in deep sea sediments (Mackin and Swider, 1989; 10–20 m away. Bacteroidetes, Epsilonproteobacteria Paull et al., 2006). The deep sea is also unusual in that it and Firmicutes were recovered primarily from whale is characterized by high pressure, low temperature and fall-associated sediments, while Gammaproteobacte- variable oxygen levels. Despite these physical and bio- ria and Planctomycetes were found primarily within chemical constraints, deep sea sediments have been reference sediments. Abundant Deltaproteobacteria shown to support abundant and diverse populations of were recovered from both sediment types, but the microorganisms (Li et al., 1999; Vetriani et al., 1999; Desulfobacteraceae and Desulfobulbaceae families Dhillon et al., 2003; Knittel et al., 2005; Inagaki et al., were observed primarily beneath the whale falls. 2006). Traditionally, however, the metabolic activity of UniFrac analysis revealed that bacterial communities these microbes has been thought to be slower than from the two whale falls (~30 km apart) clustered to shallow-living relatives (e.g. Jannasch and Wirsen, 1973), the exclusion of corresponding reference sediment and the juxtaposition of extreme physical conditions and communities, suggesting that deposition of whale fall decreased rate of carbon delivery to the seafloor make biomass is more influential on deep sea microbial the determination of what specifically controls their meta- communities than specific seafloor location. The bolic activity difficult to measure. Many deep sea bacterial bacterial population at whale-1820 at 7 months post isolates possess a high number of ribosomal operon deposition was less diverse than reference sedi- copies relative to their genome size, suggestive of oppor- ments, with Delta- and Epsilonproteobacteria and tunistic lifestyles (r-strategy and a high degree of gene Bacteroidetes making up 89% of the community. At regulation) and possibly fast response to environmental 70 months, bacterial diversity in reference sediments change (Klappenbach et al., 2000; Lauro and Bartlett, near whale-2893 had decreased as well. Over this 2008). In the laboratory, certain deep sea isolates have time, there was a convergence of each community’s demonstrated extreme resistance to starvation, and the membership at the phyla level, although lower- retained ability, after decades in some cases, for expo- taxonomic-level composition remained distinct. nential growth upon exposure to nutrients (Lauro and Long-term impact of organic carbon loading from the Bartlett, 2008). How and to what extent the structure of whale falls was also evident by elevated total organic deep sea bacterial assemblages varies in response to carbon and enhanced proteolytic activity for at least large organic accumulations in situ, however, has yet to 17–70 months. The response of the sedimentary be determined. In localized areas, stimulated microbial biomass and Received 8 June, 2009; accepted 29 July, 2009. *For correspon- activity do occur in the permanently cold depths of the dence. E-mail [email protected]; Tel. (+1) 626 395 1786; deep sea (see Jørgensen and Boetius, 2007). For Fax (+1) 626 683 0621. †Present address: Shana K. Goffredi, Biology Department, Occidental College, 1600 Campus Road, Los Angeles, example, whale falls form persistent, regionally abundant, CA 90041, USA; Email: [email protected]. organic-rich habitat islands on the deep seafloor (Smith ©2009SocietyforAppliedMicrobiologyandBlackwellPublishingLtd Deep sea bacterial community response to organic loading 345 et al., 1989; Naganuma et al., 1996; Baco and Smith, Kristensen, 1992; Moezelaar et al., 1996; Weston and 2003; Goffredi et al., 2004; Braby et al., 2007). Whale Joye, 2005). It is not known, however, how microbial carcasses deliver large amounts of organic material to the communities in the permanently cold depths of the ocean seafloor at a rate much greater than the supply of plank- respond to large organic inputs. Whale carcasses that fall tonic marine snow (Van Dover, 2000; Baco and Smith, to the seafloor (‘whale falls’) represent localized areas of 2003), thus resulting in a carbon shunt to sedimentary extreme organic enrichment in the otherwise nutrient-poor communities. The microbial ecology within these organic- deep sea and, thus, provide an opportunity to determine rich deep sea habitats has the potential to be unique, the responsiveness and adaptability of deep sea sedi- particularly with regard to interactions among microbial mentary bacteria. populations and the facilitation of specific pathways for As discrete resource patches, whale falls are thought nutrient cycling. Previous studies on whale falls suggest to contribute significantly to habitat heterogeneity, and that elevated concentrations of bioavailable carbon allow thus may contribute to the proliferation of unique micro- for the unusual coexistence of methanogenic archaea bial assemblages (Grassle and Morse-Porteous, 1987; and sulfate-reducing bacteria, possibly supported by Baco and Smith, 2003). At present there are only a enhanced rates of fermentation and associated hydrogen handful of studies investigating microbial assemblages production (Goffredi et al., 2008; Treude et al., 2009). associated with whale falls. Previous investigations Decomposition of complex organic carbon involves an include surveys of whale bone surfaces (Deming et al., assembly line of various microbial metabolisms, initiated 1997; Tringe et al., 2005) and characterizations of whale by the extracellular hydrolysis of particulate organic fall sediments, including measurements of community matter to high-molecular-weight dissolved organic com- methane production and sulfate consumption (Treude pounds, which subsequently supplies lower-molecular- et al., 2009), biomarker profiling of specific functional weight compounds (organic acids, H2) for terminal groups of methanogens and sulfate-reducing bacteria metabolism (Capone and Kiene, 1988). The specific (Naganuma et al., 1996), and molecular and biochemical groups of indigenous microorganisms responsible for this surveys of archaea and genes related to methane initial breakdown of organic carbon have not been well cycling (Goffredi et al., 2008). Collectively, these studies characterized, nor is it known how the diversity of micro- revealed an unrecognized niche for methanogenic and organisms is influenced by large organic carbon inputs to methanotrophic archaea, and reported the presence of the deep sea. sulfur-based microbial communities associated with In Monterey Canyon, two distinct whale falls within whale falls. Little attention, however, has been paid to ~50 km of shore offered a unique opportunity to better the microbial assemblages involved in early stages of understand the impact of nutrient loading on deep sea carbon degradation. microbial community structure and adaptability among various microbial groups. Events such as a whale fall Sediment geochemistry and carbon loading are expected to result in an ecologically distinct bacterial community, as compared with surrounding seafloor All sediments collected under whale falls in Monterey sediments. Following an earlier study that documented Canyon (including three additional whale falls not temporal changes in processes involving archaea (i.e. included in this study) showed significant levels of total methanogenesis; Goffredi et al., 2008), we assessed organic carbon (1–3.5% TOC, Fig. 1; Table 1; Goffredi differences in the distribution and activity of bacteria et al., 2008), relative to typical deep sea conditions involved in the hydrolytic and fermentative breakdown of (~0.1% TOC at a depth of 1200 m, Paull et al., 2006). organic carbon, as well as terminal metabolism (i.e. bac- Similarly, whale fall-impacted sediments were depleted in terial sulfate, and possible hydrogen, respiration). Sam- sulfate, relative to reference sediments (Table 1), likely a pling of two deep sea whale falls in Monterey Canyon over result of carbon degradation coupled to microbial sulfate a collective period of ~6 years allowed for the investiga- reduction. Elevated levels of methane and sulfide have tion of factors that control the spatial and temporal also previously been observed for sediments underlying