Deep ocean prokaryotic communities are remarkably malleable when facing long‐term starvation

Abstract

The bathypelagic ocean is one of the largest ecosystems on Earth and sustains half of the ocean's microbial activity. This microbial activity strongly relies on surface-derived particles, but there is growing evidence that the carbon released through solubilization of these particles may not be sufficient to meet the energy demands of deep ocean prokaryotes. To explore how bathypelagic prokaryotes respond to the absence of external inputs of carbon, we followed the long-term (1 year) dynamics of an enclosed community. Despite the lack of external energy supply, we observed a continuous succession of active prokaryotic phylotypes, which was driven by recruitment of taxa from the seed bank (i.e., initially rare operational taxonomic units [OTUs]). A single OTU belonging to Marine Group I of Thaumarchaeota, which was originally rare, dominated the microbial community for ∼ 4 months and played a fundamental role in this succession likely by introducing new organic carbon through chemolithoautotrophy. This carbon presumably produced a priming effect, because after the decline of Thaumarchaeota, the diversity and metabolic potential of the community increased back to the levels present at the start of the experiment. Our study demonstrates the profound versatility of deep microbial communities when facing organic carbon deprivation.

Higher contribution of globally rare bacterial taxa reflects environmental transitions across the surface ocean

“…First, how microbes perceive their environment at the microscale remains poorly understood (Stocker, ), and we do not even have an accurate estimate of the total microbial diversity present in a sample (Locey & Lennon, ). Second, prokaryotes can be dispersed much longer distances and can persist out of their suitable niches (dormant or inactive but capable of resuming growth, Lennon & Jones, ) for longer times than larger organisms (Langenheder et al, ; Sebastián et al, ). This, coupled to the fact that our perception of taxa occurrence is largely dependent on the sequencing resolution (Gibbons et al, ; Ruiz‐González et al, ), explains why our understanding of the ecology and mechanisms associated with microbial cosmopolitanism, dominance or rarity is far behind that of macroorganisms.…”

“…Given that closely related microbial taxa may respond differently to the same environmental drivers (Jezberová et al, ; Teeling et al, ), grouping them based on their spatio‐temporal patterns may allow partitioning communities into groups of species that share ecological strategies or similar biogeography. For example, the exploration of the temporal dynamics of individual taxa allowed identifying specific strategies shared among taxonomically different bacteria, such as opportunists that bloom under favourable conditions (i.e., Shade et al, ; Alonso‐Sáez, Díaz‐Pérez, & Morán, ; Lindh et al, ), or sequential responses to perturbations like soil rewetting or starvation (Aanderud, Jones, Fierer, & Lennon, ; Sebastián et al, ). Conversely, knowledge of the spatial distribution of individual taxa may provide insight into their persistence capacities and niche breadth, as well as into different dispersal‐related processes governing their presence.…”

“…Conversely, knowledge of the spatial distribution of individual taxa may provide insight into their persistence capacities and niche breadth, as well as into different dispersal-related processes governing their presence. This is particularly relevant in the case of prokaryotes, which are less affected by geographical barriers (e.g., Mayol et al, 2017;Reche, D'Orta, Mladenov, Winget, & Suttle, 2018;Mestre et al, 2018;Logares et al, 2018) than other organisms, and are able to persist out of their suitable niches for longer times until favourable conditions are encountered (Hervàs, Camarero, Reche, & Casamayor, 2009;Langenheder et al, 2016;Lennon & Jones, 2011;Sebastián et al, 2018).…”

Microbial Community Structure and Functionality in the Deep Sea Floor: Evaluating the Causes of Spatial Heterogeneity in a Submarine Canyon System (NW Mediterranean, Spain)

“…Interestingly, when comparing bacterial and archaeal phyla by habitat, we observed that Planctomycetes and Thaumarchaeota, both containing taxa with roles in the N cycle (Sintes et al, 2013;Restrepo-Ortiz et al, 2014;Kuypers et al, 2018), had higher richness in the open slope than in the canyon. Part of the microbial richness observed may also act as seed microbes or opportunists, actively changing their abundances as a response to environmental situations matching their functional requirements (Sebastián et al, 2018). These functional requirements displayed differences along habitats and sediment layers.…”

“…Indeed, deep-sea benthic microbial communities are generally more diverse than pelagic or open ocean surface waters (Zinger et al, 2011;Lindh et al, 2017). Still, studies in the marine realm mainly focused on pelagic ecosystems (e.g., Galand et al, 2010;Sunagawa et al, 2015;Sebastián et al, 2018). Large-scale patterns of deep-sea microbes seem to indicate that communities are vulnerable to temperature shifts, and very susceptible to changes in trophic characteristics and 'food' inputs (Danovaro et al, 2016).…”