Rapid changes in coastal ocean microbiomes uncoupled with shifts in environmental variables

Abstract

Summary Disturbances, here defined as events that directly alter microbial community composition, are commonly studied in host‐associated and engineered systems. In spite of global change both altering environmental averages and increasing extreme events, there has been relatively little research into the causes, persistence and population‐level impacts of disturbance in the dynamic coastal ocean. Here, we utilize 3 years of observations from a coastal time series to identify disturbances based on the largest week‐over‐week changes in the microbiome (i.e. identifying disturbance as events that alter the community composition). In general, these microbiome disturbances were not clearly linked to specific environmental factors and responsive taxa largely differed, aside from SAR11, which generally declined. However, several disturbance metagenomes identified increased phage‐associated genes, suggesting that unexplained community shifts might be caused by increased mortality. Furthermore, a category 1 hurricane, the only event that would likely be classified a priori as an environmental disturbance, was not an outlier in microbiome composition, but did enhance a bloom in seasonally abundant phytoplankton. Thus, as extreme environmental changes intensify, assumptions of what constitutes a disturbance should be re‐examined in the context of ecological history and microbiome responses.

Microbial Response to Natural Disturbances: Rare Biosphere often plays a role

“…However, more than half of these populations returned to rarity one or two weeks after each disturbance, consistent with the concept of conditionally rare taxa (CRT) defined by Shade and colleagues [7] and also the results of amplicon based analysis of same samples [22]. Such conditionally rare taxa may therefore provide resilience to the system undergoing disturbances and our approach here quantified this contribution in terms of relative abundance of the total community.…”

“…These results suggested that there were more carbon compounds in the surface seawater during this warming event compared to pre-disturbance sample, and microbial populations that were more efficient in utilizing those carbon gained a competitive advantage over those that lacked these pathways (e.g., abundant to rare MAGs). Amplicon based analysis also showed consistent results: a “spring bloom” indicating overturn in the phytoplankton was obvious based on the amplicon datasets [22]. However, two weeks after the event, 14 of the MAGs that had become abundant from rare during the event became rare again (77.8% of the category) while 11 MAGs that became rare from abundant became abundant again (66.7% of the category), revealing that the sampled microbial communities were resilient.…”

“…For each season in each year, 3 samples were sequenced representing non-disturbance, disturbance, and post-disturbance samples of disturbance events. Disturbance events were identified as significant changes compared to the seasonal microbial community composition and structure based on 16S rRNA gene amplicon sequencing [22] ( Figure S1 , Table S1). We also looked at the actually environmental parameters that might have driven those changes among the parameters measured.…”

“…Water samples were collected as part of the Piver's Island Coastal Observatory (PICO) time series adjacent to the Beaufort Inlet, Beaufort, NC, USA (34°71.81'N, 76°67.08'W) on a weekly basis [22]. Here, we sequenced 19 samples from January 2011 to December 2013 that represented the winter, summer, and spring seasons.…”

A Gulf Stream frontal eddy harbors a distinct microbiome compared to adjacent waters

“…Similarly, microbiomes from stable environments may be more sensitive to environmental changes [9,10]. However, in aquatic ecosystems, establishing antecedent environmental conditions is particularly challenging due to factors including water movement, unmeasured disturbances and environmental parameter seasonality [11][12][13]. Further, although dispersal limitation is assumed be reduced in aquatic systems compared to other systems, such as soils, oceanographic features such as steep frontal gradients between water parcels or vertical stratification can limit dispersal [14], and thus constrain microbiome composition [15].…”