Species invasions shift microbial phenology in a two-decade freshwater time series

Abstract

Invasive species impart abrupt changes on ecosystems, but their impacts on microbial communities are often overlooked. We paired a 20 y freshwater microbial community time series with zooplankton and phytoplankton counts, rich environmental data, and a 6 y cyanotoxin time series. We observed strong microbial phenological patterns that were disrupted by the invasions of spiny water flea ( Bythotrephes cederströmii ) and zebra mussels ( Dreissena polymorpha ). First, we detected shifts in Cyanobacteria phenology. After the spiny water flea invasion, Cyanobacteria dominance crept earlier into clearwater; and after the zebra mussel invasion, Cyanobacteria abundance crept even earlier into the diatom-dominated spring. During summer, the spiny water flea invasion sparked a cascade of shifting diversity where zooplankton diversity decreased and Cyanobacteria diversity increased. Second, we detected shifts in cyanotoxin phenology. After the zebra mussel invasion, microcystin increased in early summer and the duration of toxin production increased by over a month. Third, we observed shifts in heterotrophic bacteria phenology. The Bacteroidota phylum and members of the acI Nanopelagicales lineage were differentially more abundant. The proportion of the bacterial community that changed differed by season; spring and clearwater communities changed most following the spiny water flea invasion that lessened clearwater intensity, while summer communities changed least following the zebra mussel invasion despite the shifts in Cyanobacteria diversity and toxicity. A modeling framework identified the invasions as primary drivers of the observed phenological changes. These long-term invasion-mediated shifts in microbial phenology demonstrate the interconnectedness of microbes with the broader food web and their susceptibility to long-term environmental change.

Increased anoxia following species invasion of a eutrophic lake

“…However, in Lake Mendota no water clarity change was observed with the subsequent zebra mussel invasion (Spear et al 2021), and we did not observe an associated change in anoxia or phytoplankton biomass. Dreissenids are known to shift phytoplankton community composition (Naddafi et al 2007), and Rohwer et al (2023a) did observe an earlier seasonal timing of Cyanobacteria onset in the microbial community post-zebra mussels; however, note that our lake season "spring mixed" differs from the "spring" season in Rohwer et al (2023a) in that "spring mixed" also includes a large portion of clearwater phase. Nonetheless, our finding that Cyanobacteria and green algae increased along with diatoms, by maintaining but not increasing their proportion of total phytoplankton biomass, holds true with or without the zebra mussel years included.…”

“…A longer anoxia duration extends the period of reduced fish habitat due to oxythermal stress in Lake Mendota (Magee et al 2019), as well as the season of cyanotoxin production (Rohwer et al 2023a). We attribute an anoxic factor increase of 11 d (corresponding to an increase of hypolimnetic anoxic volume of 19 Million m 3 ) to a spiny water flea irruption in Lake Mendota.…”

“…The reduction in Daphnia abundance caused a water clarity decline due to reduction in Daphnia grazing pressure on phytoplankton (Walsh et al 2016a). This shortened the duration and intensity of Lake Mendota's spring clearwater phase (Matsuzaki et al 2020) due to higher diatom biomass (Walsh et al 2018), and an earlier appearance of Cyanophyta (Cyanobacteria) during clearwater phase (Rohwer et al 2023a).…”

Nitrogen dynamics and fixation control cyanobacterial abundance, diversity, and toxicity in Lake of the Woods (USA, Canada)

“…Upon reaching near uniform water column temperatures (July -August, SI Figure 2), cyanobacteria become the dominant taxa observed, comprising roughly 15% of the total microbial community. The shift in abundance is commiserate with typical cyanobacterial growth, as water temperatures and light availability increase (Havens et al, 2003;Rohwer et al, 2023). The diversity of dominant cyanobacterial ASVs also increase as we see Dolichospermum, Snowella, Microcystis, Aphanizomenon, and different Synechococcus ASVs all being present and at different abundance based on sampling station (Figure 5B).…”

Mixing‐driven changes in distributions and abundances of planktonic microorganisms in a large, oligotrophic lake

“…These microorganisms are phylogenetically diverse, relying on an array of metabolic strategies that include chemotrophy, phototrophy, autotrophy, heterotrophy, and mixotrophy (e.g., Zwart et al 2002; Newton et al 2011; Caliz and Casamayor 2014). Lake microorganisms are also responsive to environmental perturbations, making them sentinels of both progressive and abrupt changes to lake ecosystems (e.g., De Wever et al 2005; Cabello‐Yeves et al 2018; Rohwer et al 2023).…”