Spatial organization of the kelp microbiome at micron scales

Abstract

15Macroalgae are colonized by complex and diverse microbial communities that are distinct from 16 those on inert substrates, suggesting intimate symbioses that likely play key roles in both 17 macroalgal and bacterial biology. Canopy-forming kelp fix teragrams of carbon per year in 18 coastal kelp forest ecosystems, yet little is known about the structure and development of their 19 associated microbial communities. We characterized the spatial organization of bacterial 20 communities on blades of the canopy-forming kelp Nereocystis luetkeana using fluorescence in 21 situ hybridization and spectral imaging with a probe set combining phylum, class and genus-22Importance 35 The microbial community coating the surfaces of macroalgae may play a key but underexplored 36 role both in the biology of the macroalgal host and in the biogeochemistry of the coastal ocean. 37We show that photosynthetic blades of the canopy-forming kelp Nereocystis luetkeana host a 38 complex microbial biofilm that is both dense and spatially differentiated. Microbes of different 39 taxa are in intimate cell-to-cell contact with one another; microbial cells invade the interior of 40 kelp cells as well as cover their external surfaces; and a subset of the surface microbiota projects 41 into the water column. These results highlight the potential for metabolic interactions between 42 key members of the kelp microbiome as well as between microbes and their host. The dense 43 layer of microbes coating the surface of the kelp blade is well-positioned to mediate interactions 44 between the host and surrounding organisms and to modulate the chemistry of the surrounding 45 water column. 46 the microbiome and condition of habitat-forming kelp.

Oxygen metabolism shapes microbial settlement on photosynthetic kelp blades compared to artificial kelp substrates

“…As demonstrated previously (Weigel and Pfister, 2019; Ramirez‐Puebla et al ., 2020), N. luetkeana blade base and tip microbial biofilms had significantly different microbial community structure (Table 1; Fig. 2A).…”

“…Granulosicoccus sp . reaches high densities on the tip of N. luetkeana blades, with up to 9 × 10 6 cells cm −2 , but only sparse cells are visible on new tissue at the base of the blade (Ramirez‐Puebla et al ., 2020). While we cannot differentiate between colonization of these taxa and performance differences post‐settlement (cell growth, differential survival), the presence of Granulosicoccus sp .…”

“…Macroalgae known as kelp (order Laminariales) play a vital role in coastal ecosystems, creating kelp forest habitat and fixing tremendous amounts of carbon, yet we know little about microbial community assembly on kelps. Photosynthetic blade tissues of the canopy‐forming kelp Nereocystis luetkeana host an abundant and spatially structured microbiome of 10 7 –10 8 cells cm −2 (Ramirez‐Puebla et al ., 2020). Despite high cell density, the biofilm community is dominated by a few highly abundant bacterial taxa that displayed repeatable spatial structure over multiple months (Ramirez‐Puebla et al ., 2020) and persisted over large geographical distances (Weigel and Pfister, 2019).…”

“…Photosynthetic blade tissues of the canopy‐forming kelp Nereocystis luetkeana host an abundant and spatially structured microbiome of 10 7 –10 8 cells cm −2 (Ramirez‐Puebla et al ., 2020). Despite high cell density, the biofilm community is dominated by a few highly abundant bacterial taxa that displayed repeatable spatial structure over multiple months (Ramirez‐Puebla et al ., 2020) and persisted over large geographical distances (Weigel and Pfister, 2019). As an annual species, N. luetkeana rapidly grows from a microscopic gametophyte to a massive sporophyte during the spring and summer, becoming one of the largest primary producers in the ocean by mid‐summer.…”

Probing Patterning in Microbial Consortia with picCASO: a Cellular Automaton for Spatial Organisation

“…Natural microbial communities exhibit spatial organisation in various niches. Examples include methanogens in mesophilic and thermophilic sludge granules (Sekiguchi et al, 1999), archaea in methane seep sediment (Dekas et al, 2014), nitrifying bacteria in soil aggregates (Nishio and Furusaka, 1970), the kelp bacterial community (Ramirez-Puebla et al, 2020) and the plant rhizosphere (Steidle et al, 2001). Spatial patterning is also observed in the human gut (Tropini et al, 2017), oral (Shrivastava et al, 2018) and skin (Bouslimani et al, 2015) microbiomes, where it is also hypothesized to have functional implications.…”