Archaea and Bacteria - Their Macroecological Drivers in Benthic Deep-Sea Ecosystems

Australia: The Land Where Time Began

Archaea and Bacteria - Their Macroecological Drivers in Benthic Deep-Sea Ecosystems

The Biomass of deep-sea ecosystems is dominated by bacteria and archaea at all latitudes and they have a crucial function in global biogeochemical cycles, though their macroscale patterns and macroecological drivers are still to a large extent not known. In this paper Danovaro et al. present the results of their study that has been conducted so far investigating patterns and drivers of the distribution and structure of assemblages of benthic prokaryotes from 228 samples that were collected at latitudes comprising 34^oN to 79^oN, from depths of 400 m to 5,570 m. Danovaro et al. provide evidence that benthic bacterial and archaeal abundances increase significantly from middle latitudes to high latitudes in deep sea ecosystems, with patterns being more pronounced for archaea, particularly for Marine Group I Thaumarchaeota. It is also shown in these results that different microbial components display varying sensitivities to temperature conditions and the supply of food. Danovaro et al. have concluded that the primary effect of changing climate will impact benthic archaea from the deep sea, and this will have important consequences for global biogeochemical cycles, particularly at high latitudes.

The largest ecosystems on Earth are sediments in the deep sea, which cover about 65 % of the Earth and about 95 % of the floor of the ocean, and they control global biogeochemical cycles (Danovaro, Snelgrove & Tyler, 2014; Canals et al., 2006). A limited and episodic food supply from the water column, possibly supplemented by benthic chemoautotrophic production, largely constrains life in the deep sea sediments (Danovaro, Snelgrove & Tyler, 2014; Molari, Manini & Dell’Anno, 2013). In the deep sea sediments prokaryotes (up to 95 %) dominate the total benthic biomass, and a pivotal role in the production of carbon (either heterotrophic or chemoautotrophic), nutrient cycling and the transfer of energy to higher trophic levels (Danovaro, Snelgrove & Tyler, 2014; Jørgensen & Boetius, 2007) is played by bacteria and archaea. The concentrations of deep sea prokaryotes are highest in the surface layer of the sediments, their abundance per unit volume being from 10³ to 10⁶ times higher than in the dark portion of the water column and in the biosphere beneath the seafloor (Lipp, Morono, Inagaki & Hinrichs, 2008; Biddle et al., 2006). By the use of a modelling approach, the global biomass of prokaryotes (reported as “bacteria”) on the floor of the ocean has been estimated to be in the order of about 35 Mt of carbon (Wei et al., 2010).

Meta-analysis conducted at global scale suggests the abundance and biomass of prokaryotes remains rather constant with increasing depth of water (Wei et al., 2010; Rex et al., 2006; Danovaro et al., 2008), though significant depth-related patterns of benthic prokaryote abundance and biomass were reported by studies on a regional scale (Danovaro et al., 2000; Quéric, Soltwedel, Amtz, 2004). The lack of depth-related patterns at global scale suggests prokaryotes are also dependent on other factors acting at different spatial scales, as well as the quantity and quality (or dilution) of organic matter available in the deep sea (Boetius, Ferdelman & Lochte, 2000; Turley, 2000; Turley & Dixon, 2002; Deming & Carpenter, 2008; Giovannelli et al., 2013; Arrieta et al., 2015; Dell’Anno, Corinaldesi & Danovaro, 2015), as the food supply to benthos changes with depth, latitude, biographic region, and related productivity. High deep sea biomasses in particular have been reported in ocean regions that are highly productive, such as the North Atlantic and upwelling and polar regions, while the oligotrophic conditions support biomass values that are 1 or 2 orders of magnitude lower (such as Central Pacific and the deep Mediterranean Sea (Wei et al., 2010; Quéric, Soltwedel & Amtz, 2004). Evidence has been provided by recent studies, based on the metabolic theory, that the relative influence on deep sea organisms of chemical and thermal energy varies to a considerable extent across levels of biological organisation and the thermal energy has a major effect at lower levels of biological organisation (Canals et al., 2006). Also, prokaryotes in the deep sea can be controlled by viral infections able to abate more than 80 % of the production of biomass (Danovaro et al., 2008). It is also known that the abundance of archaea increases beneath a depth of 1,000 m and can equal the abundance of bacteria in the deeper portion of the water column and in the subsurface of the deep sea sediments. However, the factors that explain such shifts in relative importance of archaea and bacteria are still largely no known (Lipp, Morono, Inagaki & Hinrichs, 2008; Biddle et al., 2006; Karner, DeLong & Karl, 2011; Lloyd, May, Kevorkian & Steen, 2013). Overall, according to Danovaro et al. knowledge of the patterns and drivers that control the distributions of bacteria and archaea in sediments in the deep sea is completely insufficient to understand fully their ecology and their response to multiple stressors, which include the effects of global change that is predicted for the coming decades.

In this study Danovaro et al. investigated the macroecology of bacteria and archaea in the surface layer of deep sea sediments by the use of an intensive and highly replicated sampling strategy at the macroscale. 228 samples were collected from 58 benthic sites in the deep sea, which spanned from 34^oN – 79^oN encompassing different physical-chemical and trophic characteristics (such as from the Arctic to the North Atlantic to the Mediterranean basin, with temperature deltas greater than 10^oC at the same depths), and at depths that ranged from about 400 m – 5,570 m.

Danovaro et al. designed this study to provide insights into:

i) The factors that drive the distribution of benthic bacteria and archaea and, within the domain Archaea, of Marine Group I (MG-I) Thaumarchaeota and MG-II Euryarchaeaota, representing the dominant archaeal groups in the surface of the sediments from the deep sea (Durbin & Teski, 2011; Orcutt, Sylvan, Knab & Edwards, 2011), and

ii) The different sensitivity of bacteria and archaea to trophic and thermohaline conditions that are changing to forecast their potential response to global changes.

Danovaro et al. suggest their results point the increasing importance of benthic archaea at high latitudes. Also revealed by their findings, bacteria and archaea respond with different sensitivity to shifts in temperature and changes in the supply of food, showing a higher sensitivity or archaea, and particularly the MG-I Thaumarchaeota, to thermal energy changes. It is suggested by the findings of this study that global climate change will have important consequences on the structure and distribution of assemblages of prokaryotes from the deep sea, with profound implications on global biogeochemical cycles.

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