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Microbiology , Volume 1, a quarterly 23, Number The O journal of of Common Patterns Observed in Community Structure ceanography S

By David Emerson and Craig L. Moyer ociety. © 2010 by The O ceanography S

Abstract. Much interest has been generated by the discoveries of Introduction ceanography S ociety. A associated with seamounts. The volcanically active portion of these undersea Microbial is remarkable for its resil- mountains hosts a remarkably diverse range of unusual microbial , from ience to extremes of temperature, pH, Permission is reserved. ll rights granted to in teaching copy this and research. for use article R ociety. S black smokers rich in to cooler, diffuse, -rich hydrothermal vents. As and , as well its ability to persist such, seamounts potentially represent hotspots of microbial diversity, yet our and thrive using an amazing number end all correspondence to: [email protected] Th e O or understanding of the microbiology of seamounts is still in its infancy. Here, we of organic or inorganic food sources. discuss recent work on the detection of microbial communities and the Nowhere are these traits more evident observation that specific community groups may be indicative of specific geochemical than in the deep . Much of the scenarios, such as iron and sulfur cycling. These observations are based on the deep seafloor consists of cold, relatively metabolisms predicted by phylogenetic characteristics exhibited by the dominant static sedimentary environments where populations found within these microbial communities as compared to the closest heterotrophic microbes exist in signifi- related isolate found in culture. Therefore, these studies combine the use of both cant numbers, but conditions remain

cultivation-dependent and -independent analyses. Cultivation-independent studies relatively unchanged over long periods ceanography S were primarily completed using cloning and sequencing techniques targeting small of time. Mid-ocean associated subunit ribosomal gene (SSU rDNA) biomarkers along with similar biomolecular with diverging plate boundaries are often ociety, P tools like terminal-restriction fragment length polymorphism (T-RFLP) and sites of high-temperature hydrothermal quantitative polymerase chain reaction (Q-PCR), which allow for the determination venting and host many chemoauto- O B ox 1931, R

of phylotypes (analogous to ). We discuss the notion of Zetaproteobacteria trophic microbes; however, these systems epublication, systemmatic reproduction,

and/or being the most common members of hydrothermal are more homogeneous with respect M D 20849-1931, USA ockville, habitats associated with seamounts exhibiting volcanic activity. Another noneruptive to their physical and chemical proper- seamount scenario is also examined, for example, , an ties than vent systems associated with active forearc mud . volcanic arcs and backarcs (Takai et al., .

148 Oceanography Vol.23, No.1 2006), for example, seamounts. The driven by hotspots or microbiology relevant to seamount enhanced heterogeneity of seamount- plumes within ’s crust (see Staudigel studies is the capacity for microbes to hosted hydrothermal systems repre- and Clague, 2010). The Hawaiian live in the deep subsurface. The organic sents a dynamic range of habitats, in the and the in and inorganic chemical reactions, as well providing for the growth of a remarkable the are spectacular exam- as the geological processes associated diversity of microbes. ples of hotspots. Because our knowledge with microbial populations in the deep First and foremost, underwater about the role of seamounts as biogeo- subsurface , are interlinked, but volcanoes create seamounts, and the chemical foci for microbial activity is in little is known of the complexity of those intense volcanism at actively growing its infancy, it is instructive to consider linkages (, 1992; Whitman et al., seamounts results in a variety of hydro- another seamount-associated microbial 1998). Furthermore, we are only begin- thermal vent environments. Although that derives from fundamentally ning to realize both the phylogenetic these settings account for only a small different geological processes. diversity of microbes, and the extent of fraction of all seamounts, the hydro- The importance of hydrothermal their metabolic activities in these deep thermal venting offers the potential to vents associated with deep ocean crustal biosphere . Drilling proj- fuel novel life forms. Older seamounts spreading centers as havens for microbial ects done in deep mines on land have that exhibit reduced volcanism, or are activity has fundamentally changed how revealed surprising microbial communi- dormant, may still be conduits for fluid we view life on Earth, and enlightened ties living kilometers below the surface exchange between the rock mantle our thinking about other places in and taking advantage of energy sources subsurface and the ocean (Wheat our solar system where life might also derived from interactions of with et al., 2004). These fluids may also feed exist. The iconic features of these sites basement rock minerals (White et al., both deep subsurface and/or benthic are black smokers billowing super- 1998; Chivian et al., 2008). In the ocean, (bottom-dwelling) microbial communi- heated water charged with iron sulfide deep-sea drilling into old ties (Cowen et al., 2003; Huber et al., minerals, as well as dense communi- has revealed and living 2006). Finally, even dormant seamounts ties of macrofauna largely fueled by up to hundreds of meters below the that rise to appreciable depths above the symbiotic relationships with bacteria seafloor (Parkes et al., 2000; Jørgensen ocean floor (i.e., > 1000 m) can impact that provide energy for their hosts using and Boetius, 2007). The extent of micro- ocean currents and mixing, potentially sulfide-rich emanating from the organisms living in is less resulting in stimulation of microbial vents. The discovery of these deep-sea well understood because drilling into communities that feed off the enriched ecosystems has reshaped our thinking and recovering good samples from hard, nutrients (see Lavelle and Mohn, 2010). and research agenda regarding extreme fractured rock is much more challenging This latter possibility applies to active oases of life in the . Some of the than from ocean sediments. Here, seamounts as well. most notable findings from over three seamounts constitute an opportunity There are estimated to be over decades of research on hydrothermal for future studies. First, they represent 100,000 seamounts that reach a kilometer vents are the extension of the thermal extensions of Earth’s crust above the or more above the seafloor (see Wessel limit for life (Takai et al., 2008) as well seafloor, in essence making basement et al., 2010). This large number illustrates as the discovery of a host of bacteria rocks more available for sampling. the potential scope of seamounts to and archaea with novel anaerobic and Second, seamounts may act as perme- provide and impact habitats for marine aerobic metabolisms that take advantage able conduits for exchange of fluids microbes. The majority of seamounts are of unique suites of energy sources (both between the ocean and oceanic crust associated with tectonic processes taking autotrophic and heterotrophic) derived (see Fisher and Wheat, 2010). Could place in Earth’s crust, for example, from the combination of , it be that seamounts represent a new arcs that have chains of undersea moun- temperature, and pressure at these sites frontier for making discoveries about tains that result from converging plates. (Karl, 1995; Nakagawa and Takai, 2008). the diversity and abundance of microbial Another source of seamounts is undersea Another emerging aspect of life in the ocean?

Oceanography March 2010 149 Sizing Up Seamount active hydrothermal venting at young 24 seamounts ( 1). By comparison, Microbiology with seamounts (Emerson and Moyer, 2002; there have been hundreds of papers a Microbial Tour of Edwards et al., 2005; Templeton et al., investigating the different aspects of Seamounts 2009). Thus, active -arc the microbiology of circulation through the oceanic volcanoes typify hydrothermal systems centers. Nonetheless, this work illustrates crust aided by seamount-supported that provide abundant nutrient-rich the diversity of habitats that may exist at permeable pathways is conducive to fluids on which microbial communities seamounts, which, in turn, illustrates the microbiological activity because of can live and grow (Figure 1). However, variety of geochemical and hydrological the large amounts of nutrient-rich surprisingly little is known about the conditions that make many seamounts fluids that flow through these relatively microbiology of seamounts, especially in unique. It is too early to make any small volumes of permeable crust terms of community structure and diver- definitive statements about the types of (Edwards et al., 2005; Staudigel et al., sity. We compiled a summary of much microbial communities that might be 2008). Microbial biofilms may develop of the work that has been published found at seamounts, especially given on fresh , or dense microbial to date using culture-independent the incredible diversity of seamount mats (sometimes a meter or more microbial investigations, and found ecosystems. Nonetheless, some patterns thick) may form in close proximity to only 19 papers that have focused on with respect to the distribution of

Figure 1. Cross section of a typical submarine arc volcano with an active hydrothermal system. As ascends, water and gases contained in magma exsolve and enter the deep hydrothermal system as pressure is released. Cold seawater (blue arrows) perme- ates the volcano and becomes heated by the hot rock near the magma body. Hybrid hydrothermal fluids (red arrows), derived from seawater and magmatic gas and fluid, buoyantly rise to the summit while altering the (white = alteration). Fluids discharged at the seafloor rise tens to hundreds of meters before they spread laterally in a hydrothermal plume. Local currents disperse the plume, which carries various dissolved and particulate chemical species derived from the magma and the volcanic rock. Courtesy of Cornel de Ronde, GNS Science

150 Oceanography Vol.23, No.1 microbes that thrive at seamounts are this issue [Staudigel et al., 2010]). Karl levels of ferrous iron (50 to 750 µM) in emerging. We take a brief tour of the et al. (1988) made the first discovery of the vent effluent (Wheat et al., 2000). seamounts that have been studied, all seamount-associated, Fe-rich microbial In addition, the summit (presently in the Pacific Ocean, to illustrate the mats, showing bacteria with a dominant at a depth of 956 m) is in the diversity of habitats that exist and the sheathlike morphology occurring near minimum zone, so seawater O2 concen- diversity of microbes that live in those the summit at Pele’s Vents. An eruption trations are only 10–15% of saturated habitats (Figure 2). at Lō`ihi in 1996 led to the destruc- seawater (Glazer and Rouxel, 2009). tion of Pele’s Vents and the formation The initial microbiology study Lō`ihi Seamount of Pele’s Pit, a 300-m-deep pit crater Lō`ihi is a seismically active subma- with multiple actively venting sites David Emerson (demerson@bigelow. rine volcano and the youngest (Duennebier et al., 1997). The forma- org) is Senior Research Scientist, seamount in the Hawaiian Island tion of luxuriant Fe-rich microbial mats, Bigelow Laboratory for Ocean Sciences, chain; it is located 35 km southeast along with the conspicuous absence of West Boothbay Harbor, ME, USA. of the big island of Hawai`i with its large benthic macrofauna, is most likely Craig L. Moyer is Professor, Biology summit rising nearly 4 km above the due to the relatively high concentrations Department, Western Washington seafloor (see Spotlight 3 on page 72 of of dissolved CO2 (300 mM) and enriched University, Bellingham, WA, USA.

Table 1. Seamount culture-independent microbial investigations into in situ community structure and diversity

Geological Dominant Microbiology/ Seamount(s) Location References Setting Predicted Physiology Type‡ Rassa et al., 2009 Near Hawai`i, Zetaproteobacteria/FeOB Lō`ihi Hotspot Emerson and Moyer, 2002 Central North Pacific Epsilonproteobacteria/HSOB Moyer et al., 1995* Juan de Fuca , Epsilonproteobacteria/HSOB Huber et al., 2003 Axial Hotspot Northeast Pacific Zetaproteobacteria/FeOB Kennedy et al., 2003 Near , Epsilonproteobacteria/HSOB Sudek et al., 2009 Vailulu’u Hotspot Central South Pacific Zetaproteobacteria/FeOB (detected) Staudigel et al., 2006 Kato et al., 2009 Izu-Bonin Arc, Epsilonproteobacteria/HSOB Suiyo Higashi et al., 2004 Northwest Pacific /SOB Sunamura et al., 2004 Mariana Arc, Zetaproteobacteria/FeOB Davis and Moyer, 2008 Mariana Arc Island Arc Western Pacific Epsilonproteobacteria/HSOB Nakagawa et al., 2006 Near Tonga, Forget et al., in press Tonga Arc Island Arc Zetaproteobacteria/ FeOB Southwest Pacific Langley et al., 2009 Epsilonproteobacteria/HSOB Hodges and Olsen, 2009 Near New Zealand, Gammaproteobacteria/SOB Kermadec Arc Island Arc Takai, et al., 2009 Southwest Pacific Deltaproteobacteria/SRB Stott et al., 2008 Zetaproteobacteria/FeOB (detected) Crenarchaeota; Marine Group I & South Chamorro Serpentine Near , Marine Benthic Group B Curtis et al., 2009 and Muds Mariana Forearc, Euryarchaeota; Methanobacteria & Mottl et al., 2003 Mariana Forearc (ultramafic) Western Pacific Methanosarcinales/AMO (implicated) ‡ FeOB = iron-oxidizing bacteria. HSOB = -oxidizing (anaerobic) or sulfur-oxidizing (aerobic) bacteria. SOB = sulfur-oxidizing bacteria. SRB = sulfur- reducing bacteria; AMO = anaerobic oxidation. * First publication to detect both Epsilonproteobacteria (PVB OTU 2) and Zetaproteobacteria (PVB OTU 4) at a .

Oceanography March 2010 151 Axial


Mariana Arc Loihi South Chamorro

Vailulu’u Tonga Arc

Kermadec Arc

Figure 2. Pacific Ocean bathymetric map showing the locations where seamounts have been microbiologically investigated. These include (north to south): , , Lō`ihi Seamount, the Mariana Arc (n = 8), South Chamorro Seamount and Mariana Forearc (n = 7), Vailulu’u Seamount, the Tonga Arc (n = 2), and the Kermadec Arc (n=3). Image reproduced with permission from the GEBCO world map (http://www.gebco.net/)

at Lō`ihi, which used a cultivation- could represent a novel, sixth candidate many of the microbial mats at Lō`ihi, independent approach, was conducted class of (Emerson and and are an easily identified diagnostic prior to the 1996 eruption and showed Moyer, 2002; Emerson et al., 2007). indicator that Fe-oxidizing bacteria that the class Epsilonproteobacteria This conclusion was based on the are present (Figure 3). (PVB OTU 2) dominated the isolation of a novel genus and species, More recently, it has been shown that surrounding microbial mats and that Mariprofundus ferrooxydans, from an Zetaproteobacteria dominate vent-site members of the newly discovered class iron-rich mat at Lō`ihi. M. ferrooxydans colonies in and around Lō`ihi, though Zetaproteobacteria (PVB OTU 4) is a chemoautotrophic, neutrophilic colonization by Epsilonproteobacteria were also present (Moyer et al., 1995). Fe-oxidizing bacterium that gains its is also possible, most notably at higher- Phylum Proteobacteria is the largest, energy for growth by oxidizing ferrous temperature (> 40°C) vents, demon- most diverse, and well-studied bacte- (Fe2+) to ferric (Fe3+) iron, and fixes strating both spatial and temporal rial phylum, with representatives found CO2. Furthermore, as it grows, it heterogeneity among these microbial in almost all habitats and metabolic produces a stalklike structure composed mat communities (Rassa et al., 2009). conditions on Earth. It consists of primarily of Fe-oxyhydroxides, the waste An extensive analysis of multiple five recognized classes, including product of the Fe-oxidation reaction mat communities sampled from Epsilonproteobacteria. As a result of that remains behind after the cells are Lō`ihi using the DNA fingerprinting subsequent studies at Lō`ihi, it was gone (Emerson et al., 2007). These stalk- technique known as terminal restric- demonstrated that Zetaproteobacteria like structures are a common feature of tion fragment length polymorphism

152 Oceanography Vol.23, No.1 Figure 3. Morphotypes of Fe-oxidizing bacteria commonly observed at seamounts. (A) A light micrograph of Mariprofundus ferrooxydans, showing the twisted iron oxyhydroxide stalk with two cells, denoted by arrows, growing at the ends. (B) A light micrograph of an unknown organism that forms tubular iron oxide structures; the fluorescent dye image shows two cells present at the apical end of the structure, which is formed as the cells grow. (C) A transmission elec- tron microscopy image of the same organism as shown in B; note that each time the cell divides the structure bifurcates. (D) A sheath-forming Fe-oxidizing bacterium; most of the sheaths are empty tubes of iron oxyhydroxides formed by filaments of cells that grow within them.(D) is reproduced with permission (Emerson and Moyer, 2002)

(T-RFLP) has revealed that there appear with members of S-oxidizing bacteria for example, iron-encrusted stalks to be two distinct community types, (Epsilonproteobacteria) but still retain similar to those of Zetaproteobacteria Lō`ihi Groups 1 and 2; the iron-based some of the Zetaproteobacteria. (Kennedy et al., 2003). Multiple micro- Group 1 is essentially dominated by bial mat samples from across Axial’s Zetaproteobacteria and the sulfur-based Axial Seamount have been examined using Group 2 by Epsilonproteobacteria Although Axial Seamount is located T-RFLP with the majority dominated (Figure 4). Their distributions seem along the central portion of the Juan by Epsilonproteobacteria and a few to be linked to both geochemistry and de Fuca Ridge (a mid-ocean ridge dominated by Zetaproteobacteria temperature, with Group 1 common spreading center), it also lies at the (data not shown). Surprisingly, this fits at lower-temperature vents (median eastern end of the Cobb-Eickelberg the pattern seen at Lō`ihi Seamount temperature = 23°C) where there are seamount chain. Axial originated at the in terms of two distinct groups of fewer overall community members and , which generates bacterial-dominated community types Group 2 found at higher-temperature without a typical deep mantle chemical (e.g., Figure 4); however, in this location, vents (median temperature = 77°C) signature (see Spotlight 1 on page 38 the Epsilonproteobacteria were acting exhibiting a higher diversity of detect- of this issue [Chadwick et al., 2010]; as the primary colonizers at a majority able populations. We have correlated Rhodes et al., 1990). This seamount of vent sites shortly after an eruptive these results with the Group 1 commu- was intensely studied after an eruptive event that occurred in 1998 (Moyer and nities associated with vents that have event in 1998 (Embley et al., 1999), and Engebretson, 2002). higher levels of dissolved Fe2+ and members of the Epsilonproteobacteria Group 2 communities with both high were shown to dominate diffuse flow Vailulu’u Seamount 2+ H2S and Fe concentrations (data vents (Huber et al., 2003). Microbial Vailulu’u marks the current position of not shown). We hypothesize that samples from other diffuse-flow the Samoan hotspot in the southwestern Group 1 communities are enhanced vent sites in the caldera analyzed by Pacific Ocean and exhibits active volca- with members of Fe-oxidizing bacteria light microscopy, scanning electron nism and hydrothermal venting that (Zetaproteobacteria), and that the microscopy (SEM), and X-ray diffraction includes Fe-oxide rich floc, but also Group 2 communities are enhanced (XRD) showed distinct morphologies, sulfidic vents (see Spotlight 8 on page

Oceanography March 2010 153 Figure 4. Unweighted Pair Group Method with Arithmetic mean (UPGMA)/product- moment cluster analysis of 55 terminal-restriction fragment length poly- morphism bacterial community fingerprints using eight restriction digest treatments on each sample. Two groups of communities were identified and designated “Lō`ihi Group 1” and “Lō`ihi Group 2.” Colored labels indicate samples taken in the same year. Ambient temperature for summit area of Lō`ihi Seamount is 4.0°C. Scale bar is the Pearson product moment correlation r-value X 100.

154 Oceanography Vol.23, No.1 164 of this issue [Koppers et al., 2010]; chemoautotrophic species of bacteria backarc (Elsaied et al., 2007). Many Staudigel et al., 2006). Microbial samples that can use hydrogen as an energy novel members of these gene families from Vailulu’u have been analyzed source (Takai et al., 2003; Nakagawa were discovered at both sites, suggesting using both cultivation-dependent and et al., 2003), as well as an archaeon that that gene exchange between different -independent approaches. Standard can grow anaerobically with hydrogen bacteria at these sites could potentially clone library analysis with small subunit and thiosulfate (Mori et al., 2008). Other be very common. Interestingly though, ribosomal gene (SSU rDNA) biomarkers microbial studies have included an the results indicated that the two found that the majority of clones repre- examination of the hydrothermal plume different vent communities harbored sented Epsilonproteobacteria, though within the caldera, which identified two quite different sets of integron genes that Zetaproteobacteria were also detected dominant phylotypes of putative sulfur- were not necessarily compatible with (Sudek et al., 2009). In addition, a oxidizing bacteria, the SUP01 group, one another. This observation suggests diverse fungal community, including belonging to Epsilonproteobacteria, that lateral gene transfer may take place several species of yeast, was found and the SUP05 group, in the class between populations within a vent site, associated with iron mats as well as Gammaproteobacteria (Sunamura et al., but that gene transfer between geograph- with basaltic rock surfaces at Vailulu’u 2004). These phylotypes were distinct ically separated vent communities would (Connell et al., 2009). Unlike Lō`ihi, the from those common in the surrounding not happen as readily. This lack of lateral complex circulation patterns created seawater and accounted for up to 66% of gene transfer is in contrast with antibi- by Vailulu’u’s summit crater provide the bacteria in the hydrothermal plume. otic-resistant genes carrying integrons, habitat for a much more diverse and This large percentage suggests that the where disparate environmental popula- abundant macrofaunal community, hydrodynamics of the vent plume within tions have been shown to have common including and eels. One result the caldera create an incubator for these integron functions (Elsaied et al., 2007). of these flow patterns is the existence of two groups of microbes. Another micro- a “moat of death” where fish and other bial study at Suiyo used a series of novel Mariana Arc Seamounts larger animals become entrapped in catheter-type in situ growth chambers The recent expeditions anoxic water and suffocate, providing a inserted into subsurface boreholes after to multiple seamounts in the Mariana food source for anaerobic bacteria. The excavation with a portable submarine Arc made several exciting discoveries specific nutrient dynamics that support driller. In this case, a diverse array of that helped in the establishment of the the macrofauna, including the role of phylotypes from Epsilonproteobacteria new Marianas Trench Marine National bacterial primary production, have yet to were found (Higashi et al., 2004). Monument by the US government. be fully understood at Vailulu’u. An extensive examination of During these expeditions, scientists borehole and vent fluids detected observed, for the first time, a deep-sea Suiyo Seamount Gammaproteobacteria (including eruption at Brimstone Pit on Northwest Suiyo Seamount is an active submarine Thiomicrospira and Alcanivorax) in all Rota-1, found pools of black-encrusted volcano located on the volcanic front samples, while multiple samples also molten sulfur at Daikoku, witnessed of the Izu-Bonin Arc, western Pacific exhibited Epsilonproteobacteria as well the overlap between chemosynthetic Ocean, near Japan. It has a 200–300-m as a diverse array of potentially seawater- filamentous microbial mats covering deep caldera at its summit with many entrained bacterial phylotypes (Kato photosynthetic encrusting red algae and active hydrothermal vents rich in et al., 2009). Another study compared at Mat City near the summit of East and methane that the diversity and distribution of inte- Diamante (at a depth of only 200 m), and have recently been accessed through grase and integron genes (generally sampled white flocculent microbial mats shallow drilling (Ishibashi et al., 2007). thought to be responsible for lateral gene next to white smoker chimneys venting

A number of novel thermophilic transfer between unrelated bacterial liquid CO2 droplets at Champagne Vent bacteria and archaea have been isolated groups) at Suiyo Seamount and at the on Northwest Eifuku (see Spotlight 1 on from this seamount, including new Fryer site (aka Pika site) of the Mariana page 38 of this issue [Chadwick et al.,

Oceanography March 2010 155 2010]; Embley et al., 2007). In a recent (Nakagawa et al., 2006). Combined, M. ferrooxydans, supporting the assump- microbial study of 25 microbial commu- both of these microbial studies show a tion that these are biogenic iron oxides nities from 18 different hydrothermal high degree of phylogenetic diversity (Langley et al., 2009). Molecular micro- systems located at seven Mariana Arc as well as putative metabolic poten- bial analysis of similar samples from volcanoes, a remarkable diversity of tial across the Epsilonproteobacteria. both Volcanoes 1 and 19 detected the vent environments was These data also fit the general pattern presence of multiple Zetaproteobacteria found, including black smokers (220°C), that either Epsilonproteobacteria phylotypes, representing a high degree white smokers rich in CO2, vents with or Zetaproteobacteria dominate the of diversity within this group. In addi- high sulfide concentrations, as well majority of seamount vent microbial tion, these Fe-oxidizing bacteria were as iron-rich vents (Davis and Moyer, communities. Figure 5 shows some most abundant at Volcano 1, where sedi- 2008). Molecular fingerprinting analysis characteristic habitats ments were richer in Fe and contained found that the community composition dominated by either Zetaproteobacteria more crystalline forms of Fe oxides at each vent was unique, indicating a (Figure 5A and 5B) or those dominated (Forget et al., in press). substantial degree of diversity in the by Epsilonproteobacteria (Figure 5C microbial populations that inhabit and 5D). Overall, the Mariana Arc and Kermadec Arc Seamounts these ecosystems; however, the majority backarc support ecosystems that repre- The Kermadec-Tonga Arcs, together of the communities examined were sent a bacterial biodiversity hotspot the longest submarine arc system on chemosynthetic and either dominated are thought to result from the complex the planet, contain a series of recently by Epsilonproteobacteria (Mariana geochemistry of these hydrothermal explored seamounts (deRonde et al., Cluster III) or by Zetaproteobacteria systems driven by the heterogeneity of 2001, 2007). Microbial samples have (Mariana Cluster I) as determined by the subducting source material coupled been collected at , from T-RFLP. Interestingly, even though with the enhanced volcanic activity of the caldera vent field, and at the lower conditions at these seamounts were the region (Davis and Moyer, 2008). cone site. At the caldera vent field, the sometimes extreme, bacteria were exteriors of high-temperature (up to always dominant over archaea, Tonga Arc Seamounts 290°C) black smoker chimneys were with none of the communities Manned dives along dominated by variable communities of containing more than 13% archaea the Tonga Arc revealed two shallow- bacteria, including a majority of putative (Davis and Moyer, 2008). water volcanoes. Volcano 19 exhibited sulfur-oxidizing Epsilonproteobacteria In a previous Mariana Arc study, relatively high-temperature venting and Gammaproteobacteria (Takai et al., dense microbial mats were observed (245–265°C) in a depth range of 2009). A single piece of covering white-smoker sulfur chimneys 385–540 m and in some cases chim- covered with elemental sulfur and white in TOTO caldera, of Paton-Masala neys that had a distinctive “flamelike” microbial mats was collected at the Seamount, with temperatures up to discharge caused by an instantaneous lower cone site from 67°C vent effluent 170°C. Samples collected from the phase separation upon the release of and analyzed using standard molecular chimney surface and interior, and from vent fluids. Volcano 1 exhibited more microbial techniques. In this study, the an in situ colonization system indicated widespread diffuse venting (30–70°C), most abundant phylotypes detected that the microbial communities were though both had extensive areas with were from the class Deltaproteobacteria dominated by Epsilonproteobacteria filamentous microbial mats associated (most closely related to - that were either hydrogen and/ with Fe-oxyhydroxide mineral crusts reducing bacteria). However, 5% of or sulfur oxidizers or anaerobic (Stoffers et al., 2006). Samples from both this clone library was represented by hydrogen-oxidizing, sulfur-reducing locations were composed primarily of Epsilonproteobacteria phylotypes (Stott chemoautotrophs. This study also two-line ferrihydrite, and transmission et al., 2008). Another recent micro- showed that these microbial communi- electron microscopy (TEM) revealed bial study from two more seamounts ties contained no more than 2% archaea structures similar to those formed by (Clark and Tangaroa) on the southern

156 Oceanography Vol.23, No.1 Figure 5. Photographs of microbial mats collected by remotely operated vehicle. (A) Iron-oxide-encrusted microbial mat at Yellow Top Vent, Northwest Eifuku. (B) Small chimneys and iron oxide microbial mats inside Pele’s Pit Crater at Upper Hiolo Vents, Lō`ihi. (C) White smoker vents covered with microbial mats at Champagne Vents, Northwest Eifuku. (D) White microbial mats covering rocks at Vent, Northwest Rota-1.

Kermadec Arc, revealed extensive zones Fe-floc and two samples microbial mats), or perhaps the of flocculent iron oxides on the order showed that a majority of these samples Fe-oxidizing Zetaproteobacteria are of tens to hundreds of square meters. contained detectable Zetaproteobacteria only active in rapidly accreting mats Morphologically, these microbial mats peaks. These findings from the (Hodges and Olsen, 2009). resembled the biogenic oxides found at southern Kermadec Arc suggest Lō`ihi and elsewhere. Phylotypes of the that we may not fully understand South Chamorro and Other Zetaproteobacteria were detected in each the story of iron-oxidizing bacte- Mariana Forearc Seamounts of the three mats examined; however, rial communities associated with The Mariana forearc is comprised of the clone libraries were dominated seamounts. Either there may be a group a series of serpentine mud volcanoes (67% of the total number of clones) by of as-of-yet uncultured Fe-oxidizers formed between the members of the Epsilonproteobacteria. that are Epsilonproteobacteria and the that lies to its T-RFLP fingerprinting analysis of five (facilitating the formation of Fe-floc west (Fryer et al., 1999).

Oceanography March 2010 157 reactions within the subducting plate seawater and highly alkaline, with pH dissolved sulfide with nearly no sulfate, transform the overriding plate into a up to 12.5 (see Spotlight 9 on page 174 which is attributed to both anaerobic hydrated composite of serpentinite, of this issue [Wheat et al., 2010]; methane oxidation (AMO) and sulfate mud, and fluids that extrudes from - Mottl et al., 2003, 2004). reduction in a microbial habitat over- derived conduits, resulting in giant mud South Chamorro Seamount has active whelmingly dominated by archaea volcanoes. These mud volcanoes reach summit springs (Figure 6). This area was (Mottl et al., 2003). Mariana forearc sizes up to 50 km in diameter and 2 km the focus of an Ocean Drilling Program mud volcanoes thus provide a unique in height (Fryer et al., 2006). In addi- (ODP) investigation (Leg 195, Site 1200) biogeochemical view into the process of tion, springs often form (as a byproduct into the structure and diversity of the devolatization of a subducting slab and of the fluid, attributed to the microbial populations existing near the the serpentinization processes within sediment compaction and dehydra- seamount surface and at depth below the the overriding plate as mechanisms tion process) and deliver water to the seafloor. In general, these highly alkaline for fueling subsurface communities of seafloor that is typically fresher than fluids also contain elevated levels of extremophilic archaea. This habitat also

Figure 6. Summit springs at South Chamorro Seamount showing bathymodiolid mussels present. Photo taken from submersible Shinkai 6500 view port. Courtesy of Patty Fryer, University of Hawai`i

158 Oceanography Vol.23, No.1 provides an excellent opportunity for to be abundant in the surface habitats Although most are autotrophs, they can microbial investigation of phylogenetic sampled at seamounts, although they also be mixotrophs and occasionally diversity and ecological significance in are far more abundant in the interior heterotrophs (Campbell et al., 2006). an extreme subsurface environment of high-temperature chimneys and For example, the phylotypes most often representing the upper pH limit for life anaerobic subsurface fluids at volcani- found at Lō`ihi are from within the (Takai et al., 2005). cally active seamounts (Huber et al., Sulfurovum and groups A recent molecular microbial study revealed new populations of archaea that exist at the seafloor in serpenti- nized muds from South Chamorro …seamounts potentially represent Seamount. Archaeal communities hotspots of microbial diversity, yet our from seven Mariana forearc seamounts were assessed with T-RFLP, while two understanding of the microbiology of sites atop South Chamorro were also “ seamounts is still in its infancy. investigated using clone library analysis. Though a bacterium (Marinobacter alkaliphilus) was previously isolated from ODP Site 1200 seafloor muds 2002; Takai et al., 2009). A notable (sulfur oxidizers), although Nitratiruptor (Takai et al., 2005), no bacteria were exception are the mud volcanoes from group (hydrogen-oxidizing, sulfur-” detected using PCR-based molecular Mariana forearc, which represent some reducer) phylotypes have also been methods. Novel Crenarcheaota phylo- of the most extremely alkaline habitats detected (Moyer et al., 1995; Rassa types, from within Marine Group I on Earth and appear to be dominated et al., 2009; Figure 7). and Marine Benthic Group B, as well by unusual archaea (Curtis et al., The emerging discovery of as Euryarcheaota phylotypes from the 2009). Overall, microbial community Zetaproteobacteria associated with Methanobacteria and Methanosarcinales, patterns must reflect the underlying diffuse vents that are rich in avail- were detected. T-RFLP fingerprinting geochemistry that is driven by seamount able Fe2+ is intriguing. On the basis of revealed that similar archaeal commu- geologic processes; for example, neither morphology, it has been recognized since nities from Big Blue and Blue Moon Epsilonproteobacteria or Zetaproteo- the 1980s that conspicuous iron-oxide- seamounts were nearly identical to the bacteria are common members of the encrusted stalks, presumed to be of South Chamorro ODP Hole 1200E site, seawater surrounding seamounts. biogenic origin, were commonly found which was hypothesized to correlate As mentioned earlier, the in flocculent iron oxyhydroxide deposits with active summit spring habitats Epsilonproteobacteria are comprised collected from modern and ancient (Curtis et al., 2009). of a large breadth and depth of phylo- hydrothermal sites (Juniper and Fouquet, genetic diversity. Significant effort has 1988). It was the isolation of M. ferrooxy- Emerging Patterns gone into cultivating representatives dans and analysis of its SSU rDNA (as Regarding Community for each of the various groups that well as other evolutionary conserved Structure have been described using cultivation- genes) that suggested it represented a There is growing evidence, as summa- independent approaches based on the novel class of Proteobacteria (Emerson rized in Table 1, that Zetaproteobacteria analysis of SSU rDNA clone libraries. et al., 2007). While this group of and/or Epsilonproteobacteria are the A recent review finds that all cultures microbes was initially thought to be very most common members of surface characterized as hydrothermal-vent- rare, follow-up studies are suggesting that hydrothermal habitats associated associated Epsilonproteobacteria either Zetaproteobacteria can be quite abun- with volcanically active seamounts. oxidize reduced sulfur or reduce sulfur dant at seamount habitats rich in iron. Somewhat surprisingly, archaea tend not while oxidizing hydrogen or formate. The fact that M. ferrooxydans is in culture

Oceanography March 2010 159 does not mean that we have described mats at Lō`ihi also provide tantalizing organism divides, the tube bifurcates all the important Zetaproteobacteria. evidence that other “morphotypes” into a characteristic Y shape, illustrated Indeed, it appears that M. ferrooxydans of Fe-oxidizers exist. One common in Figure 3B and 3C. These structures may represent a lineage that is rela- morphotype is an unusual flattened are common in several of the mats at tively minor at most sites (Figure 3A). tubular iron-oxide structure with a single Lō`ihi, and in some cases outnumber Morphological information from the cell growing at the apical end. When the other morphotypes of Fe-oxidizers.




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Figure 3D. Although this organism looks where hydrothermal processes prevail very much like the common freshwater compared to mid-ocean ridges? Is Acknowledgments Fe-oxidizer Leptothrix ochracea, we have iron-oxidation a more important We thank Clara Chan for use of the not identified any phylotypes related to process at seamounts than at ridge- TEM image used in Figure 3C. This members of the class Betaproteobacteria, axis spreading centers? work was supported in part by grants to which Leptothrix belongs. It is possible • Are seamounts windows into a from the National Science Foundation that these marine sheathed Fe-oxidizers subsurface world? How important (MCB-0348330 to DE; MCB-0348734 represent a case of convergent evolu- are subseafloor circulation paths for and OCE-0727086 to CLM) and by tion, where organisms that are quite the redistribution of microbes? Can funding from the NASA different phylogenetically have found microbes themselves influence these Institute (to DE). a common strategy to grow with iron. patterns by altering the subsurface It is also quite possible, perhaps even flow regimes? References likely, that not all Zetaproteobacteria are • To what extent do water-column Campbell, B.J., A.S. Engel, M.L. Porter, and K. Takai. 2006. The versatile ε-proteobacteria: Fe-oxidizers, but that some might use hydrodynamics associated with Key players in sulphidic habitats. other substrates for growth. seamounts influence microbial Reviews Microbiology 4:458–468. Chadwick, W.W., D.A. Butterfield, R.W. Embley, community structure and dynamics V. Tunnicliffe, J.A. Huber, S.L. Nooner, and Opportunities for through their influence on ocean D.A. Clague. 2010. Spotlight 1: Axial Seamount. Microbial Research at Oceanography 23(1):38–39 dynamics and changes in nutrient Chivian, D., E.L. Brodie, E.J. Alm, D.E. Culley, Seamounts Abound distribution patterns? P.S. Dehal, T.Z. DeSantis, T.M. Gihring, In general, our understanding of the • How important are seamounts to A. Lapidus, L.-H. Lin, S.R. Lowry, and others. 2008. Environmental genomics reveals a forces that shape microbial community global marine geomicrobiology and single-species ecosystem deep within Earth. structure within a given environment what is their role in altering the crust Science 322:275–278. Connell, L., A. Barrett, A. Templeton, and are in a state of flux, be it the human and , including iron H. Staudigel. 2009. Fungal diversity asso- gut, marsh sediment, or the ocean’s and sulfur cycling in the ocean? How ciated with an active deep sea volcano: Vailulu’u Seamount, Samoa. Journal of . The same can be said might seamounts affect ocean acidifi- Geomicrobiology 26:597–605. even more emphatically of seamounts, cation and the global cycle? Cowen, J.P., S.J. Giovannoni, F. Kenig, because they are poorly studied These types of questions illustrate H.P. Johnson, D. Butterfield, M.S. Rappe, M. Hutnak, and P. Lam. 2003. Fluids from compared to these other environments. both how limited our understanding is aging ocean crust that support microbial life. Nonetheless, seamounts have the poten- of undersea microbial ecosystems, and Science 299:120–123. Curtis, A.C., C.G. Wheat, P. Fryer, and C.L. Moyer. tial to make good natural laboratories also how much potential remains for 2009. Mariana forearc serpentine mud for studying basic problems having to do significant new discoveries in marine volcanoes harbor novel communities of extre- mophilic Archaea. Poster Abstracts: IODP with and . microbiology. In addition to contrib- New Ventures in Exploring Scientific Targets Because they tend to be geographically uting new knowledge about fundamental (INVEST), September 23–25, 2009, Bremen, isolated from one another, there may processes at the ocean floor and in the Germany. Davis, R.E., and C.L. Moyer. 2008. Extreme spatial be more of a barrier for movement of subsurface, it is possible that novel and temporal variability of hydrothermal between seamounts compounds, enzymes, or organisms microbial mat communities along the Mariana Island Arc and southern Mariana back-arc than is the case in the more contiguous could be discovered from seamounts that system. Journal of Geophysical Research 113, environments of a mid-ocean ridge. would have practical applications in the B08S15, doi:10.1029/2007JB005413. deRonde, C.E.J., E.T. Baker, G.J. Massoth, Thus, seamounts could represent reposi- biotechnology, bioenergy, or bioreme- J.E. Lupton, I.C. Wright, R.A. Feely, and tories for studying the of diation sectors. It is even possible that R.R. Greene. 2001. Intra-oceanic - microbial populations. In addition, many microbes from seamounts could provide

Oceanography March 2010 161 related hydrothermal venting, Kermadec on Mariana forearc seamounts. Geochemistry, Kato, S., K. Hara, H. Kasai, T. Teramura, volcanic arc, New Zealand. Earth and Planetary Geophysics, Geosystems 7(8), Q08014, M. Sunamura, J. Ishibashi, T. Kakegawa, Science Letters 193:359–369. doi:10.1029/2005GC001201. T. Yamanaka, H. Kimura, K. Marumo, T. Urabe, deRonde, C.E.J., E.T. Baker, G.J. Massoth, Fryer, P., C.G. Wheat, and M.J. Mottl. 1999. and A. Yamagishi. 2009. Spatial distribution, J.E. Lupton, I.C. Wright, R.J. Sparks, Mariana blueschist mud volcanism: diversity and composition of bacterial commu- S.C. Bannister, M.E. Reyners, S.L. Walker, Implications for conditions within the subduc- nities in sub-seafloor fluids at a deep-sea hydro- R.R. Greene, and others. 2007. Submarine tion zone. Geology 27:103–106. thermal field of the Suiyo Seamount. Deep-Sea hydrothermal activity along the mid- Glazer, B.T., and O.J. Rouxel. 2009. Redox specia- Research Part I 56:1,844–1,855. Kermadec Arc, New Zealand: Large-scale tion and distribution within diverse iron-domi- Kennedy, C.B., S.D. Scott, and F.G. Ferris. 2003. effects on venting. Geochemistry, Geophysics, nated microbial habitats at Loihi Seamount. Ultrastructure and potential sub-seafloor Geosystems 8(7), Q07007, doi:10.1029/ Journal of Geomicrobiology 26:606–622. evidence of bacteriogenic iron oxides from 2006GC001495. Gold, T. 1992. The deep, hot biosphere. Proceedings Axial Volcano, , north- Duennebier, F.K., N.C. Becker, J. Caplan-Auerbach, of the National Academy of Sciences of the east Pacific Ocean. FEMS Microbiology D.A. Clague, J. Cowen, M. Cremer, M. Garcia, United States of America 89:6,045–6,049. Ecology 43:247–254. F. Goff, A. Malahoff, G.M. McMurtry, and Higashi, Y., M. Sunamura, K. Kitamura, Koppers, A.A.P., H. Staudigel, S.R. Hart, C. Young, others. 1997. Researchers rapidly respond to K. Nakamura, Y. Kurusu, J. Ishibashi, T. Urabe, and J.G. Konter. 2010. Spotlight 8: Vailulu’u submarine activity at Loihi Volcano, . and A. Maruyama. 2004. Microbial diversity in Seamount. Oceanography 23(1):164–165. Eos, Transactions, American Geophysical hydrothermal surface to subsurface environ- Langley, S., P. Igric, Y. Takahashi, Y. Sakai, Union 78:229–233. ments of Suiyo Seamount, Izu-Bonin Arc, using D. Fortin, M.D. Hannington, and U. Schwarz- Edwards, K.J., W. Bach, and T.M. McCollom. 2005. a catheter-type in situ growth chamber. FEMS Schampera. 2009. Preliminary characteriza- Geomicrobiology in oceanography: Microbe- Microbiology Ecology 47:327–336. tion and biological reduction of putative mineral interactions at and below the seafloor. Hodges, T.W., and J.B. Olsen. 2009. Molecular biogenic iron oxides (BIOS) from the Tonga- TRENDS in Microbiology 13:449–456.­ comparison of bacterial communities within Kermadec Arc, Southwest Pacific Ocean. Elsaied, H., H.W. Stokes, T. Nakamura, iron-containing flocculent mats associ- Geobiology 7:35–49. K. Kitamura, H. Fuse, and A. Maruyama. 2007. ated with submarine volcanoes along the Lavelle, J.W., and C. Mohn. 2010. Motion, commo- Novel and diverse integron integrase genes and Kermadec Arc. Applied and Environmental tion, and biophysical connections at deep ocean integron-like gene cassettes are prevalent in Microbiology 75:1,650–1,657. seamounts. Oceanography 23(1):90–103. deep-sea hydrothermal vents. Environmental Huber, J.A., D.A. Butterfield, and J.A. Baross. Mori, K., A. Maruyama, T. Urabe, K. Suzuki, and Microbiology 9:2,298–2,312. 2002. Temporal changes in archaeal diver- S. Hanada. 2008. Archaeoglobus infectus sp. nov., Embley, R.W., E.T. Baker, D.A. Butterfield, sity and chemistry in a mid-ocean ridge a novel thermophilic, chemolithoheterotrophic W.W. Chadwick, J.E. Lupton, J.A. Resing, subseafloor habitat. Applied and Environmental archaeon isolated from a deep-sea rock C.E.J. de Ronde, K. Nakamura, V. Tunnicliffe, Microbiology 68:1,585­–1,594. collected at Suiyo Seamount, Izu-Bonin J. Dower, and S.G. Merle. 2007. Exploring the Huber, J.A., D.A. Butterfield, and J.A. Baross. 2003. Arc, western Pacific Ocean. International submarine ring of fire, Mariana Arc–Western Bacterial diversity in a subseafloor habitat Journal of Systematic and Evolutionary Pacific. Oceanography 20(4):68–79. following a deep-sea volcanic eruption. FEMS Microbiology 58:810–816. Embley, R.W., W.W. Chadwick, D. Clague, and Microbiology Ecology 43:393–409. Mottl, M.J., S.C. Komor, P. Fryer, and C.L. Moyer. D. Stakes. 1999. 1998 Eruption of Axial Huber, J.A., H.P. Johnson, D.A. Butterfield, 2003. Deep-slab fluids fuel extremophilic Volcano: Multibeam anomalies and sea- and J.A. Baross. 2006. Microbial life in Archaea on a Mariana forearc serpentinite mud floor observations. Geophysical Research ridge flank crustal fluids. Environmental volcano: Ocean Drilling Program Leg 195. Letters 26:3,425–3,428. Microbiology 8:88–99. Geochemistry, Geophysics, Geosystems 4(11), Emerson, D., and C.L. Moyer. 2002. Neutrophilic Ishibashi, J., K. Marumo, A. Maruyama, 9009, doi:10.1029/2003GC000588. Fe-oxidizing bacteria are abundant at the and T. Urabe. 2007. Direct access to the Mottl, M.J., C.G. Wheat, P. Fryer, J. Gharib, and Loihi Seamount hydrothermal vents and play a sub-vent biosphere by shallow drilling. J.B. Martin. 2004. Chemistry of springs across major role in Fe oxide deposition. Applied and Oceanography 20(1):24–25. the Mariana forearc shows progressive devola- Environmental Microbiology 68:3,085–3,093. Jørgensen, B.B., and A. Boetius. 2007. Feast and tilization of the subducting plate. Geochimica et Emerson, D., J.A. Rentz, T.G. Lilburn, R.E. Davis, famine: Microbial life in the deep-sea bed. Cosmochimica Acta 68:4,915–4,933. H. Aldrich, C. Chan, and C.L. Moyer. 2007. Nature Reviews Microbiology 5:770–781. Moyer, C.L., and J.J. Engebretson. 2002. A novel lineage of Proteobacteria involved in Juniper, S.K., and Y. Fouquet. 1988. Filamentous Colonization by pioneer populations of epsilon- formation of marine Fe-oxidizing microbial mat iron-silica deposits from modern and Proteobacteria and community succession at communities. PLoS ONE 2:e667, doi:10.1371/ ancient hydrothermal sites. Canadian mid-ocean ridge hydrothermal vents as deter- journal.pone.0000667. Mineralogist 26:859–869. mined by T-RFLP analysis. Eos, Transactions, Fisher, A.T., and C.G. Wheat. 2010. Karl, D.M. 1995. Ecology of free-living, hydro- American Geophysical Union, Fall Meeting Seamounts as conduits for massive fluid, thermal vent microbial communities. Supplement, 83, Abstract V11C-12. heat, and solute fluxes on ridge flanks. Pp. 35–124 in Microbiology of Deep-Sea Moyer, C.L., F.C. Dobbs, and D.M. Karl. Oceanography 23(1):74–87. Hydrothermal Vents. D.M. Karl, ed., CRC Press, 1995. Phylogenetic diversity of the bacte- Forget, N.L., S.A. Murdock, and S.K. Juniper. In Boca Raton, FL. rial community from a microbial mat at press. Bacterial diversity in Fe-rich hydro- Karl, D.M., G.M. McMurtry, A. Malahoff, and an active, hydrothermal vent system, Loihi thermal sediments at two South Tonga Arc M.O. Garcia. 1988. Loihi Seamount, Hawaii: Seamount, Hawaii. Applied and Environmental submarine volcanoes. Geobiology. A mid-plate volcano with a distinctive hydro- Microbiology 61:1,555–1,562. Fryer P., J. Gharib, K. Ross, I. Savov, and M.J. Mottl. thermal system. Nature 335:532–535. 2006. Variability in serpentinite mudflow mechanisms and sources: ODP drilling results

162 Oceanography Vol.23, No.1 Nakagawa, S., and K. Takai. 2008. Deep-sea vent characterization of a novel microbial commu- Wessel, P., D.T. Sandwell, and S.-S. Kim. chemoautotrophs: Diversity, biochemistry and nity at a hydrothermal vent at Brothers 2010. The global seamount census. ecological significance. FEMS Microbiology Volcano, Kermadec arc, New Zealand. Oceanography 23(1):24–33. Ecology 65:1–14. Journal of Geophysical Research 113, B08S06, Wheat, C.G., P. Fryer, K. Takai, and S. Hulme. Nakagawa, S., K. Takai, K. Horikoshi, and Y. Sako. doi:10.1029/2007JB005477. 2010. Spotlight 9: South Chamarro Seamount. 2003. Persephonella hydrogeniphila sp. nov., Sudek, L.A., A.S. Templeton, B.M. Tebo, and Oceanography 23(1):174–175. a novel thermophilic, hydrogen-oxidizing H. Staudigel. 2009. Microbial ecology of Fe Wheat, C.G., H.W. Jannasch, J.N. Plant, bacterium from a deep-sea hydrothermal vent (hydr)oxide mats and basaltic rock from C.L. Moyer, F.J. Sansone, and G.M. McMurty. chimney. International Journal of Systematic and Vailulu’u Seamount, . 2000. Continuous sampling of hydro- Evolutionary Microbiology 53:863–869. Geomicrobiology Journal 26:581–596. thermal fluids from Loihi Seamount after Nakagawa, T., K. Takai, Y. Suzuki, H. Hirayama, Sunamura, M., Y. Higashi, C. Miyako, J. Ishibashi, the 1996 event. Journal of Geophysical U. Konno, U. Tsunogai, and K. Horikoshi. 2006. and A. Maruyama. 2004. Two Bacteria Research 105:19,353–19,367. Geomicrobiological and character- phylotypes are predominant in the Suiyo Wheat, C.G., M.J. Mottl, A.T. Fisher, D. Kadko, ization of a novel deep-sea hydrothermal system Seamount hydrothermal plume. Applied and E.E. Davis, and E. Baker. 2004. Heat flow at the TOTO caldera in the Mariana Volcanic Environmental Microbiology 70:1,190–1,198. through a basaltic outcrop on a sedimented Arc. Environmental Microbiology 8:37–49. Takai, K., C.L. Moyer, M. Miyazaki, Y. Nogi, young ridge flank. Geochemistry, Geophysics, Parkes, R.J., B.A. Cragg, and P. Wellsbury. 2000. H. Hirayama, K.H. Nealson, and K. Horikoshi. Geosystems 5(12), Q12006, doi:10.1029/ Recent studies on bacterial populations and 2005. Marinobacter alkaliphilus sp. nov., a 2004GC000700. processes in subseafloor sediments: A review. novel alkaliphilic bacterium isolated from White, D.C., T.J. Phelps, and T.C. Onstott. 1998. Hydrogeology Journal 8:11–28. subseafloor alkaline serpentine mud from What’s up down there? Current Opinion in Rassa, A.C., S.M. McAllister, S.A. Safran, and Ocean Drilling Program Site 1200 at South Microbiology 1:286–290. C.L. Moyer. 2009. Zeta-Proteobacteria Chamorro Seamount, Mariana Forearc. Whitman, W.B., D.C. Coleman, and W.J. Wiebe. dominate the colonization and formation of 9:17–27. 1998. : The unseen majority. microbial mats in low-temperature hydro- Takai, K., S. Nakagawa, A.-L. Reysenbach, Proceedings of the National Academy of Sciences thermal vents at Loihi Seamount, Hawaii. J. Hoek. 2006. Microbial ecology of mid-ocean of the United States of America 95:6,578–6,583. Geomicrobiology Journal 26:623–638. ridges and back-arc basins. Pp. 185–213 Rhodes, J.M., C. Morgan, and R.A. Liias. 1990. in Back-Arc Spreading Systems: Geological, Geochemistry of Axial Seamount lavas: Biological, Chemical, and Physical Interactions. Magmatic relationship between the Cobb D.M. Christie, C.R. Fisher, S.M. Lee, and Hotspot and the Juan de Fuca Ridge. Journal of S. Givens, eds, Geophysical Monograph Geophysical Research 95:12,713–12,733. Series 166, American Geophysical Union, Staudigel, H., and D.A. Clague. 2010. The geolog- Washington, DC. ical history of deep-sea volcanoes: Biosphere, Takai, K., S. Nakagawa, Y. Sako, and K. Horikoshi. hydrosphere, and lithosphere interactions. 2003. Balnearium lithotrophicum gen. nov., sp. Oceanography 23(1):58–71. nov., a novel thermophilic, strictly anaerobic, Staudigel, H., H. Furnes, N. McLoughlin, hydrogen-oxidizing chemolithoautotroph N.R. Banerjee, L.B. Connell, and A. Templeton. isolated from a black smoker chimney in 2008. 3.5 billion years of glass bioalteration: the Suiyo Seamount hydrothermal system. Volcanic rocks as a basis for microbial life? International Journal of Systematic and Earth-Science Reviews 89:156–176. Evolutionary Microbiology 53:1,947–1,954. Staudigel, H., S.R. Hart, A. Pile, B.E. Bailey, Takai, K., K. Nakamura, T. Toki, U. Tsunogai, E.T. Baker, S. Brooke, D.P. Connelly, L. Haucke, M. Miyazaki, J. Miyazaki, H. Hirayama, C.R. German, I. Hudson, and others. 2006. S. Nakagawa, T. Nunoura, and K. Horokoshi. Vailulu’u Seamount, Samoa: Life and death on 2008. Cell proliferation at 122°C and

an active . Proceedings of isotopically heavy CH4 production by the National Academy of Sciences of the United hyperthermophilic methanogen under high- States of America 103:6,448–6,453. pressure cultivation. Proceedings of the National Staudigel, H., C.L. Moyer, M.O. Garcia, Academy of Sciences of the United States of A. Malahoff, D.A. Clague, and A.A.P. Koppers. America 105:10,949–10,954. 2010. Spotlight 3: Lō`ihi Seamount. Takai, K., T. Nunoura, K. Horikoshi, T. Shibuya, Oceanography 23(1):72–73. K. Nakamura, Y. Suzuki, M. Stott, G.J. Massoth, Stoffers, P., T.J. Worthington, U. Schwarz- B.W. Christenson, C.E.J. deRonde, and others. Schampera, M.D. Hannington, G.J. Massoth, 2009. Variability in microbial communities R. Hekinian, M. Schmidt, L.J. Lundsten, in black smoker chimneys at the NW caldera L.J. Evans, R. Vaiomo’unga, and T. Kerby. 2006. vent field, Brothers Volcano, Kermadec Arc. Submarine volcanoes and high-temperature Geomicrobiology Journal 26:552–569. hydrothermal venting on the Tonga arc, Templeton, A.S., E.J. Knowles, D.L. Eldridge, Southwest Pacific. Geology 34:453–456. B.W. Arey, A.C. Dohnalkova, S.M. Webb, Stott, M.B., J.A. Saito, M.A. Crowe, P.F. Dunfield, B.E. Bailey, B.M. Tebo, and H. Staudigel. 2009. S. Hou, E. Nakasone, C.J. Daughney, A seafloor microbial hosted within A.V. Smirnova, B.W. , K. Takai, incipient ferromanganese crusts. Nature and M. Alam. 2008. Culture-independent Geoscience 2:872–876.

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