Sinking particles promote vertical connectivity in the ocean microbiome

Abstract

SignificanceProkaryotes dominate the living biomass and the biological diversity of the ocean, one of the largest ecosystems on earth. The sinking of particles is a widespread mechanism that transports materials to the deep ocean, with a significant role in the global carbon cycle. Whether this process constitutes a global dispersal pathway for prokaryotic diversity connecting surface communities to those in the dark ocean has never been tested. Here we show that surface and deep-sea prokaryotic communities are strongly connected, constituting a vast oceanic metacommunity where local assemblages are linked through the transport of sinking particles. This vertical dispersal, mediated mainly by the largest sinking particles, emerges as a fundamental process shaping the assembly and biogeography of deep ocean prokaryotic communities.

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

“…Indeed, we observed that OTUs originally categorized as bimodal or logistic based on their presence in surface free‐living communities, largely increased their relative abundances at other depth layers and size‐fractions (Supporting Information Figure ). This indicates that globally rare surface taxa may become abundant in these other habitats, in agreement with the recently reported strong connectivity between surface and deep microbial communities via sinking particles or water masses movement (Luna et al, ; Mestre et al, ; Wilkins et al, ). Exploring taxa distributions across different environments may thus help determine how differently environmental transitions or boundaries affect the distribution of each taxon.…”

“…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. In this context, the identification of bacterial spatial “behaviours” across large spatial scales is emerging as a promising way to gain insight into microbial biogeography drivers (Mestre et al, ; Niño‐García et al, ; Ruiz‐González et al, , ). For example, the SpAD approach allowed discovering that hydrologic transport from rivers explained the presence of most rare bacteria in boreal lakes, but at the same time inoculated taxa able to thrive in lake conditions (Niño‐García et al, ).…”

“…For example, the SpAD approach allowed discovering that hydrologic transport from rivers explained the presence of most rare bacteria in boreal lakes, but at the same time inoculated taxa able to thrive in lake conditions (Niño‐García et al, ). However, the origin and the causes underlying the huge reservoir of rare diversity and its role in the ocean are still poorly understood (Logares et al, ; Ser‐Giacomi et al, ) and we are only starting to comprehend how processes such as dispersal may shape the biogeography of marine microorganisms (Mestre et al, ; Wilkins, Sebille, Rinthoul, Lauro, & Cavicchioli, ).…”

“…We focused on the 0.2–3 μm fraction, which represents mostly free‐living bacteria. In addition, at eight of these stations (asterisks in Figure ), the prokaryotic communities inhabiting deeper layers and larger size‐fractions were also characterized by sequentially filtering 10 L of water from the rosette through 20, 5.0, 3.0, 0.8 and 0.2 µm 47 mm pore‐size filters (20 μm pore‐size filter from GE Water and Process Technologies [Trevose, PA, USA] and the rest from Millipore [Billerica, MA, USA]), resulting in size fractions that represent free‐living prokaryotes (0.2–0.8 µm), as well as various particle‐attached fractions (0.8–3; 3–5; 5–20 and 20–200 µm, see Mestre et al () for details on this particular data set). These different fractions were collected from the surface but also from the DCM, mesopelagic, and bathypelagic waters (see above).…”

Community structural differences shape microbial responses to high molecular weight organic matter

“…First, some microbial taxa may overcome dispersal limitation imposed by hydrographic or other physical barriers (Spencer‐Cervato and Thierstein, ; Galand et al, ). Oceanic dispersal of diverse plankton has been shown (Sexton and Norris, ; Malviya et al, ; Whittaker and Rynearson, ); however, such large vertical range – from surface waters to the bathypelagic realm – for the same taxon is not well‐documented, but has been observed among taxa associated with large sinking particles (Mestre et al, ). A second important point is that deep sea microbes may hydrolyze components of HMW‐OM at rates comparable to those observed in much shallower waters (Figs and ).…”