The Effect of Salmon Food-Derived DOM and Glacial Melting on Activity and Diversity of Free-Living Bacterioplankton in Chilean Patagonian Fjords

Fjord ecosystems cycle and export significant amounts of carbon and appear to be extremely sensitive to climate change and anthropogenic perturbations. To identify patterns of microbial responses to ongoing natural and human-derived changes in the fjords of Chilean Patagonia, we examined the effect of organic enrichment associated with salmon aquaculture and freshening produced by glacial melting on bacterial production (BP), extracellular enzymatic activity (EEA), and community diversity of free-living bacterioplankton. We assayed the effects of salmon food-derived dissolved organic matter (SF-DOM) and meltwaters through microcosm experiments containing waters from Puyuhuapi Fjord and the proglacial fjords of the Southern Patagonia Icefield, respectively. Rates of BP and EEA were 2 times higher in the presence of SF-DOM than in controls, whereas the addition of autochthonous organic matter derived from diatoms (D-DOM) resulted in rates of BP and EEA similar to those measured in the controls. The addition of SF-DOM also reduced species richness and abundance of a significant fraction of the representative taxa of bacterioplankton of Puyuhuapi Fjord. In the proglacial fjords, bacterioplankton diversity was reduced in areas more heavily influenced by meltwaters and was accompanied by moderate positive changes in BP and EEA. Our findings strongly suggest that SF-DOM is highly reactive, promoting enhanced rates of microbial activity while could be influencing the diversity of bacterioplankton communities in Patagonian fjords with a strong salmon farming activity. These findings challenge the traditional view of phytoplankton production as the primary source of labile DOM that fuels heterotrophic activity in coastal ecosystems impacted by anthropogenic organic enrichment. Given the intensive local production of salmon, we analyze the significance of this emerging source of rich “allochthonous” organic substrates for autotrophic/heterotrophic balance, carbon exportation, and hypoxia in Patagonian fjords. The effect of human DOM enrichment can be enhanced in proglacial fjords, where progressive glacial melting exerts additional selective pressure on bacterioplankton diversity.

Abundances and morphotypes of the coccolithophore <i>Emiliania huxleyi</i> in southern Patagonia compared to neighbouring oceans and Northern Hemisphere fjords

Coccolithophores are potentially affected by ongoing ocean acidification, where rising CO2 lowers seawater pH and calcite saturation state (Ωcal). Southern Patagonian fjords and channels provide natural laboratories for studying these issues due to high variability in physical and chemical conditions. We surveyed coccolithophore assemblages in Patagonian fjords during late spring 2015 and early spring 2017. Surface Ωcal exhibited large variations driven mostly by freshwater inputs. High-Ωcal conditions (max. 3.6) occurred in the Archipelago Madre de Dios. Ωcal ranged from 2.0–2.6 in the western Strait of Magellan and 1.5–2.2 in the inner channel and was subsaturating (0.5) in Skyring Sound. Emiliania huxleyi was the only coccolithophore widely distributed in Patagonian fjords (> 96 % of total coccolithophores), only disappearing in the Skyring Sound, a semi-closed mesohaline system. Correspondence analysis associated higher E. huxleyi biomasses with lower diatom biomasses. The highest E. huxleyi abundances in Patagonia were in the lower range of those reported in Norwegian fjords. Predominant morphotypes were distinct from those previously documented in nearby oceans but similar to those of Norwegian fjords. Moderately calcified forms of E. huxleyi A morphotype were uniformly distributed throughout Patagonia fjords. The exceptional R/hyper-calcified coccoliths, associated with low Ωcal values in Chilean and Peruvian coastal upwellings, were a minor component associated with high Ωcal levels in Patagonia. Outlying mean index (OMI) niche analysis suggested that pH and Ωcal conditions explained most variation in the realized niches of E. huxleyi morphotypes. The moderately calcified A morphotype exhibited the widest niche breadth (generalist), while the R/hyper-calcified morphotype exhibited a more restricted realized niche (specialist). Nevertheless, when considering an expanded sampling domain, including nearby southeast Pacific coastal and offshore waters, even the R/hyper-calcified morphotype exhibited a higher niche breadth than other closely phylogenetically related coccolithophore species. The occurrence of E. huxleyi in naturally low pH–Ωcal environments indicates that its ecological response is plastic and capable of adaptation.

Influence of Estuarine Water on the Microbial Community Structure of Patagonian Fjords

Fjords are sensitive areas affected by climate change and can act as a natural laboratory to study microbial ecological processes. The Chilean Patagonian fjords (41–56°S), belonging to the Subantarctic ecosystem (46–60°S), make up one of the world’s largest fjord systems. In this region, Estuarine Water (EW) strongly influences oceanographic conditions, generating sharp gradients of oxygen, salinity and nutrients, the effects of which on the microbial community structure are poorly understood. During the spring of 2017 we studied the ecological patterns (dispersal and oceanographic factors) underlying the microbial community distribution in a linear span of 450 km along the estuarine-influenced Chilean Patagonian fjords. Our results show that widespread microbial dispersion existed along the fjords where bacterioplankton exhibited dependence on the eukaryotic phytoplankton community composition. This dependence was particularly observed under the low chlorophyll-a conditions of the Baker Channel area, in which a significant relationship was revealed between SAR11 Clade III and the eukaryotic families Pyrenomonadaceae (Cryptophyte) and Coccomyxaceae (Chlorophyta). Furthermore, dissolved oxygen and salinity were revealed as the main drivers influencing the surface marine microbial communities in these fjords. A strong salinity gradient resulted in the segregation of the Baker Channel prokaryotic communities from the rest of the Patagonian fjords. Likewise, Microbacteriaceae, Burkholderiaceae and SAR11 Clade III, commonly found in freshwater, were strongly associated with EW conditions in these fjords. The direct effect of EW on the microbial community structure and diversity of the fjords exemplifies the significance that climate change and, in particular, deglaciation have on this marine region and its productivity.

Genetic Conservation Management of Marine Resources and Ecosystems of Patagonian Fjords

The Chilean fjord region includes many remote and poorly known areas where management plans for the marine living resources and conservation strategies are urgently needed. Few data are available about the spatial distribution of its marine invertebrate fauna, prevalently influenced by complex interactions between biotic and abiotic factors, animal behavior and human activities. Patagonian fjords are a hotspot for finfish aquaculture, elevating Chile to the world’s second producer of farmed salmon, after Norway, a condition that emphasizes the necessity to develop strategies for a sustainable aquaculture management. The present study focuses on the emblematic cold-water coral Desmophyllum dianthus, dwelling the Comau Fjord from shallow to deep waters, with the aim to illustrate population structure, demography and adaptation of the species and its potential use for the development of a sustainable conservation and management plan for human activities. The analyses of microsatellite loci of D. dianthus individuals from four sampling localities along horizontal and vertical gradients of Comau Fjord, lead to identify them as a panmictic population. The results also contributed to consider a careful examination of the synchrony between the temporal and spatial variations of environmental factors and the biological cycle of the species as key role player in the inference of autecology of the species. The discussion stresses the importance of molecular analyses as extremely helpful tools for studies focusing on remote areas and non-model organisms, where logistic difficulties and limited scientific knowledge hamper a better management and conservation of marine resources, and in particular the relevance of multidisciplinary approaches to reduce the extensive knowledge gap on the remote fjord ecosystems of Patagonia. This study also highlights the importance of oceanographic information in the entire process of the analyses and interpretation of genetic results.

Abundances and morphotypes of the coccolithophore <i>Emiliania huxleyi</i> in southern Patagonia compared to neighboring oceans and northern-hemisphere fjords

Coccolithophores are potentially affected by ongoing ocean acidification, where rising CO2 lowers seawater pH and calcite saturation state (Ωcal). Southern Patagonian fjords and channels provide natural laboratories for studying these issues due to high variability in physical and chemical conditions. We surveyed coccolithophore assemblages in Patagonian fjords during late-spring 2015 and early-spring 2017. Surface Ωcal exhibited large variations driven mostly by freshwater inputs. High Ωcal conditions (max. 3.6) occurred in the Archipelago Madre de Dios. Ωcal ranged from 2.0–2.6 in the western Strait of Magellan, 1.5–2.2 in the Inner Channel, and was sub-saturating (0.5) in Skyring Sound. Emiliania huxleyi was the only coccolithophore widely distributed in Patagonian fjords (> 96 % of total coccolitophores), only disappearing in the Skyring Sound, a semi-closed mesohaline system. Correspondence analysis associated higher E. huxleyi biomasses with lower diatom biomasses. The highest E. huxleyi abundances in Patagonia were in the lower range of those reported in Norwegian fjords. Predominant morphotypes were distinct from those previously documented in nearby oceans but similar to those of Norwegian fjords. Moderate-calcified forms of E. huxleyi A morphotype were uniformly distributed throughout Patagonia fjords. The exceptional R/hyper-calcified coccoliths, associated with low Ωcal values in Chilean and Peruvian coastal upwellings, were a minor component associated with high Ωcal levels in Patagonia. Outlying mean index (OMI) niche analysis suggested that pH/Ωcal conditions explained most variation in the realized niches of E. huxleyi morphotypes. The moderate-calcified A morphotype exhibited the widest niche-breadth (generalist), while the R/hyper-calcified morphotype exhibited a more restricted realized niche (specialist). Nevertheless, when considering an expanded sampling domain, including nearby Southeast Pacific coastal and offshore waters, even the R/hyper-calcified morphotype exhibited a higher niche breadth than other closely phylogenetically-related coccolithophore species. The occurrence of E. huxleyi in naturally low pH/Ωcal environments indicates that its ecological response is plastic and capable of adaptation.