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ABSTRACT Whether a microbe is free-living or associated with a host from across the tree of life, its existence depends on a limited number of elements and electron donors and acceptors. Yet divergent approaches have been used by investigators from different fields. The “environment first” research tradition emphasizes thermodynamics and biogeochemical principles, including the quantification of redox environments and elemental stoichiometry to identify transformations and thus an underlying microbe. The increasingly common “microbe first” research approach benefits from culturing and/or DNA sequencing methods to first identify a microbe and encoded metabolic functions. Here, the microbe itself serves as an indicator for environmental conditions and transformations. We illustrate the application of both approaches to the study of microbiomes and emphasize how both can reveal the selection of microbial metabolisms across diverse environments, anticipate alterations to microbiomes in host health, and understand the implications of a changing climate for microbial function. 

Elucidating the spatial structure of host-associated microbial communities is essential for understanding taxon-taxon interactions within the microbiota and between microbiota and host. Macroalgae are colonized by complex microbial communities, suggesting intimate symbioses that likely play key roles in both macroalgal and bacterial biology, yet little is known about the spatial organization of microbes associated with macroalgae. Canopy-forming kelp are ecologically significant, fixing teragrams of carbon per year in coastal kelp forest ecosystems. We characterized the micron-scale spatial organization of bacterial communities on blades of the kelpNereocystis luetkeanausing fluorescence in situ hybridization and spectral imaging with a probe set combining phylum-, class-, and genus-level probes to localize and identify > 90% of the microbial community.

We show that kelp blades host a dense microbial biofilm composed of disparate microbial taxa in close contact with one another. The biofilm is spatially differentiated, with clustered cells of the dominant symbiontGranulosicoccussp. (Gammaproteobacteria) close to the kelp surface and filamentousBacteroidetesandAlphaproteobacteriarelatively more abundant near the biofilm-seawater interface. A community rich inBacteroidetescolonized the interior of kelp tissues. Microbial cell density increased markedly along the length of the kelp blade, from sparse microbial colonization of newly produced tissues at the meristematic base of the blade to an abundant microbial biofilm on older tissues at the blade tip. Kelp from a declining population hosted fewer microbial cells compared to kelp from a stable population.

Imaging revealed close association, at micrometer scales, of different microbial taxa with one another and with the host. This spatial organization creates the conditions necessary for metabolic exchange among microbes and between host and microbiota, such as provisioning of organic carbon to the microbiota and impacts of microbial nitrogen metabolisms on host kelp. The biofilm coating the surface of the kelp blade is well-positioned to mediate interactions between the host and surrounding organisms and to modulate the chemistry of the surrounding water column. The high density of microbial cells on kelp blades (10⁵–10⁷cells/cm²), combined with the immense surface area of kelp forests, indicates that biogeochemical functions of the kelp microbiome may play an important role in coastal ecosystems.

 

Canopy‐forming kelps are foundational species in coastal ecosystems, fixing tremendous amounts of carbon, yet we know little about the ecological and physiological determinants of dissolved organic carbon (DOC) release by kelps. We examined DOC release by the bull kelp,Nereocystis luetkeana, in relation to carbon fixation, nutrient uptake, tissue nitrogen content, and light availability. DOC release was approximately 3.5 times greater during the day than at night. During the day,N. luetkeanablades released an average of 16.2% of fixed carbon as DOC. Carbon fixation increased with light availability but DOC release did not, leading to a lower proportion of fixed carbon released as DOC at high light levels. We found no relationship between carbon fixation and DOC release rates measured concurrently. Rather, DOC release byN. luetkeanablades declined with marginal significance as blade tissue nitrogen content increased and with experimental nitrate addition, supporting the role of stoichiometric relationships in DOC release. Using a stable isotope (¹³C) tracer method, we demonstrated that inorganic carbon is rapidly fixed and released byN. luetkeanablades as¹³DOC, within hours. However, recently fixed carbon (¹³DOC) comprised less than 20% of the total DOC released, indicating that isotope studies that rely on tracer production alone may underestimate total DOC release, as it is decoupled from recent kelp productivity. Comparing carbon and nitrogen assimilation dynamics of the annual kelpN. luetkeanawith the perennial kelpMacrocystis pyriferarevealed thatN. luetkeanahad significantly higher carbon fixation, DOC production and nitrogen uptake rates per unit dry mass. Both kelp species were able to perform light‐independent carbon fixation at night. Carbon fixation by the annual kelpN. luetkeanais as high as 2.35 kg C·m⁻²·yr⁻¹, but an average of 16% of this carbon (376 g C·m⁻²·yr⁻¹) is released as DOC. As kelp forests are increasingly viewed as vehicles for carbon sequestration, it is important to consider the fate of this substantial quantity of DOC released by canopy‐forming kelps.

 

Primary producers respond to climate directly and indirectly due to effects on their consumers. In the temperate coastal ocean, the highly productive brown algae known as kelp have both strong climate and grazer linkages. We analyzed the demographic response of the kelpPleurophycus gardneriover a 25‐year span to determine the interaction between ocean climate indicators and invertebrate infestation rates.Pleurophycushosts amphipod species that burrow in the stipe, increasing mortality. Although kelp performance is generally greater with more negative values of the Pacific Decadal Oscillation (PDO) and colder seawater temperatures,Pleurophycusshowed the opposite pattern. When we compared the 1990s, a period of positive values for thePDOand warmer sea surface temperatures, with the following decade, a period characterized by negativePDOvalues, we documented a contradictory outcome for proxies of kelp fitness. In the 1990s,Pleurophycusunexpectedly showed greater longevity, faster growth, greater reproductive effort, and a trend toward decreased amphipod infestation compared with the 2006–2012 period. In contrast, the period from 2006 to 2012 showed opposite kelp performance patterns and with a trend toward greater amphipod infestation.Pleurophycusperformance metrics suggest that some coastal primary producers will respond differently to climate drivers, particularly if they interact strongly with grazers.

 

Ocean acidification, a product of increasing atmospheric carbon dioxide, may already have affected calcified organisms in the coastal zone, such as bivalves and other shellfish. Understanding species’ responses to climate change requires the context of long‐term dynamics. This can be particularly difficult given the longevity of many important species in contrast with the relatively rapid onset of environmental changes. Here, we present a unique archival dataset of mussel shells from a locale with recent environmental monitoring and historical climate reconstructions. We compare shell structure and composition in modern mussels, mussels from the 1970s, and mussel shells dating back to 1000–2420 yearsBP. Shell mineralogy has changed dramatically over the past 15 years, despite evidence for consistent mineral structure in the California mussel,Mytilus californianus, over the prior 2500 years. We present evidence for increased disorder in the calcium carbonate shells of mussels and greater variability between individuals. These changes in the last decade contrast markedly from a background of consistent shell mineralogy for centuries. Our results use an archival record of natural specimens to provide centennial‐scale context for altered minerology and variability in shell features as a response to acidification stress and illustrate the utility of long‐term studies and archival records in global change ecology. Increased variability between individuals is an emerging pattern in climate change responses, which may equally expose the vulnerability of organisms and the potential of populations for resilience.