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Genomic signatures of Lake Erie bacteria suggest interaction in the Microcystis phycosphere.

ABSTRACT: Microbial interactions in harmful algal bloom (HAB) communities have been examined in marine systems, but are poorly studied in fresh waters. To investigate HAB-microbe interactions, we isolated bacteria with close associations to bloom-forming cyanobacteria, Microcystis spp., during a 2017 bloom in the western basin of Lake Erie. The genomes of five isolates (Exiguobacterium sp. JMULE1, Enterobacter sp. JMULE2, Deinococcus sp. JMULE3, Paenibacillus sp. JMULE4, and Acidovorax sp. JMULE5.) were sequenced on a PacBio Sequel system. These genomes ranged in size from 3.1 Mbp (Exiguobacterium sp. JMULE1) to 5.7 Mbp (Enterobacter sp. JMULE2). The genomes were analyzed for genes relating to critical metabolic functions, including nitrogen reduction and carbon utilization. All five of the sequenced genomes contained genes that could be used in potential signaling and nutrient exchange between the bacteria and cyanobacteria such as Microcystis. Gene expression signatures of algal-derived carbon utilization for two isolates were identified in Microcystis blooms in Lake Erie and Lake Tai (Taihu) at low levels, suggesting these organisms are active and may have a functional role during Microcystis blooms in aggregates, but were largely missing from whole water samples. These findings build on the growing evidence that the bacterial microbiome associated with bloom-forming algae have the functional potential to contribute to nutrient exchange within bloom communities and interact with important bloom formers like Microcystis.

SUBMITTER: Hoke AK

PROVIDER: S-EPMC8457463 | biostudies-literature | 2021

REPOSITORIES: biostudies-literature

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Genomic signatures of Lake Erie bacteria suggest interaction in the Microcystis phycosphere.

Hoke Alexa K AK Reynoso Guadalupe G Smith Morgan R MR Gardner Malia I MI Lockwood Dominique J DJ Gilbert Naomi E NE Wilhelm Steven W SW Becker Isabella R IR Brennan Grant J GJ Crider Katherine E KE Farnan Shannon R SR Mendoza Victoria V Poole Alison C AC Zimmerman Zachary P ZP Utz Lucy K LK Wurch Louie L LL Steffen Morgan M MM

PloS one 20210922 9

Microbial interactions in harmful algal bloom (HAB) communities have been examined in marine systems, but are poorly studied in fresh waters. To investigate HAB-microbe interactions, we isolated bacteria with close associations to bloom-forming cyanobacteria, Microcystis spp., during a 2017 bloom in the western basin of Lake Erie. The genomes of five isolates (Exiguobacterium sp. JMULE1, Enterobacter sp. JMULE2, Deinococcus sp. JMULE3, Paenibacillus sp. JMULE4, and Acidovorax sp. JMULE5.) were s ...[more]

PMID: 34550975

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Project description:Western Lake Erie (Laurentian Great Lakes) is prone to annual cyanobacterial harmful algal blooms (cHABs) dominated by Microcystis spp. that often yield microcystin toxin concentrations exceeding the federal EPA recreational contact advisory of 8 μg liter-1 In August 2014, microcystin levels were detected in finished drinking water above the World Health Organization 1.0 μg liter-1 threshold for consumption, leading to a 2-day disruption in the supply of drinking water for >400,000 residents of Toledo, Ohio (USA). Subsequent metatranscriptomic analysis of the 2014 bloom event provided evidence that release of toxin into the water supply was likely caused by cyanophage lysis that transformed a portion of the intracellular microcystin pool into the dissolved fraction, rendering it more difficult to eliminate during treatment. In August 2019, a similar increase in dissolved microcystins at the Toledo water intake was coincident with a viral lytic event caused by a phage consortium different in composition from what was detected following the 2014 Toledo water crisis. The most abundant viral sequence in metagenomic data sets was a scaffold from a putative member of the Siphoviridae, distinct from the Ma-LMM01-like Myoviridae that are typically documented to occur in western Lake Erie. This study provides further evidence that viral activity in western Lake Erie plays a significant role in transformation of microcystins from the particulate to the dissolved fraction and therefore requires monitoring efforts from local water treatment plants. Additionally, identification of multiple lytic cyanophages will enable the development of a quantitative PCR toolbox to assess viral activity during cHABs.IMPORTANCE Viral attack on cHABs may contribute to changes in community composition during blooms, as well as bloom decline, yet loss of bloom biomass does not eliminate the threat of cHAB toxicity. Rather, it may increase risks to the public by delivering a pool of dissolved toxin directly into water treatment utilities when the dominating Microcystis spp. are capable of producing microcystins. Detecting, characterizing, and quantifying the major cyanophages involved in lytic events will assist water treatment plant operators in making rapid decisions regarding the pool of microcystins entering the plant and the corresponding best practices to neutralize the toxin.

Project description:This study assessed the distribution, abundance, and viability of pre- and post-overwintering Microcystis sediment seed stocks in Western Lake Erie and how these variables are potentially related to past and subsequent bloom formation. We conducted a two-year spatiotemporal survey of vegetative seed stocks in Western Lake Erie, the region where annual algal blooms generally develop. Sediment was collected from 16 sites covering an area of 375 km2 and water column depths ranging from 3-9 meters. Sample collection occurred in November 2014, April 2015, November 2015, and April 2016. The abundance of total and potentially-toxic Microcystis cell equivalents were determined using quantitative polymerase chain reaction. A series of laboratory experiments using lake sediment were conducted to assess the viability of Microcystis vegetative seed stocks. Across all sampling periods, the abundance of total Microcystis in the sediment ranged from 6.6 x 10(4) to 1.7 x 10(9) cell equivalents g-1, and potentially-toxic Microcystis ranged from 1.4 x 10(3) to 4.7 x 10(6) cell equivalents g-1. The percent potentially-toxic Microcystis in the sediment ranged from <1% to 68% across all samples. Total Microcystis abundance diminished significantly over winter with densities in spring nearly 10 times less than the previous fall. However, despite cell loss from fall to spring, lab experiments demonstrated that remaining non-toxic and potentially-toxic cells were viable after the overwintering period. Further, lab grow-out experiments indicate that potentially-toxic strains recruited at a slightly higher rate than non-toxic strains, and may in part, contribute to the pattern of higher relative toxicity during early stages of the blooms. The abundance and distribution of overwintering cells did not correlate strongly to areas in the lake where subsequent summer blooms were most persistent. However, numerical analysis suggests that recruitment of benthic overwintering populations could help explain a portion of the initial rapid increase in bloom biomass and the spatial extent of this bloom initiation, particularly when recruitment is paired with subsequent growth in appropriate water column conditions.

Project description:Although evidence indicates that viruses are important in the ecology of Microcystis spp., many questions remain. For example, how does Microcystis exist at high, bloom-associated cell concentrations in the presence of viruses that infect it? The phenomenon of lysogeny and associated homoimmunity offer possible explanations to this question. Virtually nothing is known about lysogeny in Microcystis , but a metatranscriptomic study suggests that widespread, transient lysogeny is active during blooms. These observations lead us to posit that lysogeny is important in modulating Microcystis blooms. Using a classic mitomycin C-based induction study, we tested for lysogeny in a Microcystis -dominated community in Lake Erie in 2019. Treated communities were incubated with 1 mg L -1 mitomycin C for 48 h alongside unamended controls. We compared direct counts of virus-like-particles (VLPs) and examined community transcription for active infection by cyanophage. Mitomycin C treatment did not increase VLP count. Mitomycin C effectively eliminated transcription in the cyanobacterial community, while we detected no evidence of induction. Metatranscriptomic analysis demonstrated that the standard protocol of 1 mg L -1 was highly-toxic to the cyanobacterial population, which likely inhibited induction of any prophage present. Follow-up lab studies indicated that 0.1 mg L -1 may be more appropriate for use in freshwater cyanobacterial studies. These findings will guide future efforts to detect lysogeny in Microcystis blooms.ImportanceHarmful algal blooms dominated by Microcystis spp. occur throughout the world's freshwater ecosystems leading to detrimental effects on ecosystem services that are well documented. After decades of research, the scientific community continues to struggle to understand the ecology of Microcystis blooms. The phenomenon of lysogeny offers an attractive, potential explanation to several ecological questions surrounding blooms. However, almost nothing is known about lysogeny in Microcystis . We attempted to investigate lysogeny in a Microcystis bloom in Lake Erie and found that the standard protocols used to study lysogeny in aquatic communities are inappropriate for use in Microcystis studies, and perhaps freshwater cyanobacterial studies more broadly. This work can be used to design better methods to study the viral ecology of Microcystis blooms.

Dataset Information

Genomic signatures of Lake Erie bacteria suggest interaction in the Microcystis phycosphere.

Publications

Genomic signatures of Lake Erie bacteria suggest interaction in the Microcystis phycosphere.

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