Abstract
Bacteria are integral to marine carbon cycling. They transfer organic carbon to higher trophic levels and remineralise it into inorganic forms. Kelp forests are among the most productive ecosystems within the global oceans, yet the diversity and metabolic capacity of bacteria that transform kelp carbon is poorly understood. Here, we use 16S amplicon and metagenomic shotgun sequencing to survey bacterial communities associated with the surfaces of the giant kelp Macrocystis pyrifera and assess the capacity of these bacteria for carbohydrate metabolism. We find that Macrocystis-associated communities are distinct from the water column, and that they become more diverse and shift in composition with blade depth, which is a proxy for tissue age. These patterns are also observed in metagenomic functional profiles, though the broader functional groups—carbohydrate active enzyme families—are largely consistent across samples and depths. Additionally, we assayed more than 250 isolates cultured from Macrocystis blades and the surrounding water column for the ability to utilize alginate, the primary polysaccharide in Macrocystis tissue. The majority of cultured bacteria (66%) demonstrated this capacity; we find that alginate utilization is patchily distributed across diverse genera in the Bacteroidetes and Proteobacteria, yet can also vary between isolates with identical 16S rRNA sequences. The genes encoding enzymes involved in alginate metabolism were detected in metagenomic data across taxonomically diverse bacterial communities, further indicating this capacity is likely widespread amongst bacteria in kelp forests. Overall, the M. pyrifera epibiota shifts across a depth gradient, demonstrating a connection between bacterial assemblage and host tissue state.
Highlights
Heterotrophic bacteria play an essential role in the world’s oceans by metabolizing and remineralising dissolved and particulate organic carbon that would otherwise be unavailable to higher trophic levels (Azam and Malfatti, 2007)
The uncultured M. pyrifera epibiota differs strongly from the uncultured bacterial community found in the water column; while many operational taxonomic units (OTUs) are shared across these sample types their relative abundance differs markedly (Figure 1A)
Differences between water and M. pyrifera are driven in part by high abundance of Cyanobacteria in the water, but near absence on M. pyrifera, and abundant Verrucomicrobia (Persicirhabdus) and Planctomycetes (Blastopirellula) on M. pyrifera blades from middle and top depths (Figures 1A,B)
Summary
Heterotrophic bacteria play an essential role in the world’s oceans by metabolizing and remineralising dissolved and particulate organic carbon that would otherwise be unavailable to higher trophic levels (Azam and Malfatti, 2007). These interactions provide a key contribution to biogeochemical cycling by liberating refractory carbon, shuttling carbon between coastal systems (Säwström et al, 2016), and reducing the sequestration of carbon to the deep ocean (Jiao et al, 2010). Alginate Utilization in the Macrocystis Microbiome of kelp carbon is released to the environment as detritus (i.e., particulate organic carbon; Krumhansl and Scheibling, 2012), while a smaller portion is exuded as dissolved organic matter (Reed et al, 2015). Given the abundance of carbon within kelp forest ecosystems and the interdependence between bacterial metabolism and marine productivity, the kelp forest is an important system in which to study microbial carbon cycling and oceanic nutrient fluxes
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